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    The time course of molecular acclimation to seawater in a euryhaline fish

    1.Edwards, S. L. & Marshall, W. S. In Euryhaline Fishes. Fish Physiology Vol. 32 (eds Farrell Stephen, A. P. et al.) 1–44 (Academic Press, 2012).Chapter 

    Google Scholar 
    2.Evans, D. H., Piermarini, P. M. & Choe, K. P. The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev. 85, 97–177. https://doi.org/10.1152/physrev.00050.2003 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    3.Kultz, D. Physiological mechanisms used by fish to cope with salinity stress. J. Exp. Biol. 218, 1907–1914. https://doi.org/10.1242/jeb.118695 (2015).Article 
    PubMed 

    Google Scholar 
    4.Schultz, E. T. & McCormick, S. D. In Euryhaline Fishes. Fish Physiology Vol. 32 (eds Farrell, A. P. et al.) 477–533 (Academic Press, 2012).Chapter 

    Google Scholar 
    5.Scott, G. R., Richards, J. G., Forbush, B., Isenring, P. & Schulte, P. M. Changes in gene expression in gills of the euryhaline killifish Fundulus heteroclitus after abrupt salinity transfer. Am. J. Physiol. Cell Physiol. 287, C300–C309. https://doi.org/10.1152/ajpcell.00054.2004 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    6.Deane, E. E. & Woo, N. Y. Differential gene expression associated with euryhalinity in sea bream (Sparus sarba). Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1054–R1063. https://doi.org/10.1152/ajpregu.00347.2004 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    7.Scott, G. R., Claiborne, J. B., Edwards, S. L., Schulte, P. M. & Wood, C. M. Gene expression after freshwater transfer in gills and opercular epithelia of killifish: Insight into divergent mechanisms of ion transport. J. Exp. Biol. 208, 2719–2729. https://doi.org/10.1242/jeb.01688 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    8.Dymowska, A. K., Hwang, P. P. & Goss, G. G. Structure and function of ionocytes in the freshwater fish gill. Respir. Physiol. Neurobiol. 184, 282–292. https://doi.org/10.1016/j.resp.2012.08.025 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    9.Hiroi, J. & McCormick, S. D. New insights into gill ionocyte and ion transporter function in euryhaline and diadromous fish. Respir. Physiol. Neurobiol. 184, 257–268. https://doi.org/10.1016/j.resp.2012.07.019 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    10.Hsu, H. H., Lin, L. Y., Tseng, Y. C., Horng, J. L. & Hwang, P. P. A new model for fish ion regulation: Identification of ionocytes in freshwater- and seawater-acclimated medaka (Oryzias latipes). Cell Tissue Res. 357, 225–243. https://doi.org/10.1007/s00441-014-1883-z (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    11.Hwang, P. P. & Lin, L. Y. In The Physiology of Fishes Vol. 4 (eds Evans, D. H. et al.) 205–233 (CRC Press, 2013).
    Google Scholar 
    12.Evans, T. G. & Somero, G. N. A microarray-based transcriptomic time-course of hyper- and hypo-osmotic stress signaling events in the euryhaline fish Gillichthys mirabilis: Osmosensors to effectors. J. Exp. Biol. 211, 3636–3649. https://doi.org/10.1242/jeb.022160 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    13.Fiol, D. F. & Kultz, D. Osmotic stress sensing and signaling in fishes. FEBS J. 274, 5790–5798. https://doi.org/10.1111/j.1742-4658.2007.06099.x (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    14.Kultz, D. The combinatorial nature of osmosensing in fishes. Physiology (Bethesda) 27, 259–275. https://doi.org/10.1152/physiol.00014.2012 (2012).CAS 
    Article 

    Google Scholar 
    15.Komoroske, L. M. et al. Sublethal salinity stress contributes to habitat limitation in an endangered estuarine fish. Evol. Appl. 9, 963–981. https://doi.org/10.1111/eva.12385 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Foskett, J. K., Logsdon, C. D., Turner, T., Machen, T. E. & Bern, H. A. Differentiation of the chloride extrusion mechanism during seawater adaptation of a teleost fish, the cichlid Sarotherodon mossambicus. J. Exp. Biol. 93, 209–224 (1981).Article 

    Google Scholar 
    17.Katoh, F. & Kaneko, T. Short-term transformation and long-term replacement of branchial chloride cells in killifish transferred from seawater to freshwater, revealed by morphofunctional observations and a newly established “time-differential double fluorescent staining” technique. J. Exp. Biol. 206, 4113–4123. https://doi.org/10.1242/jeb.00659 (2003).Article 
    PubMed 

    Google Scholar 
    18.Uchida, K., Kaneko, T., Miyazaki, H., Hasegawa, S. & Hirano, T. Excellent salinity tolerance of mozambique tilapia (Oreochromis mossambicus): Elevated chloride cell activity in the branchial and opercular epithelia of the fish adapted to concentrated seawater. Zool. Sci. 17, 149–160. https://doi.org/10.2108/zsj.17.149 (2000).Article 

    Google Scholar 
    19.Whitehead, A., Roach, J. L., Zhang, S. & Galvez, F. Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus heteroclitus) gill. J. Exp. Biol. 215, 1293–1305. https://doi.org/10.1242/jeb.062075 (2012).Article 
    PubMed 

    Google Scholar 
    20.Mundy, P. C., Jeffries, K. M., Fangue, N. A. & Connon, R. E. Differential regulation of select osmoregulatory genes and Na+/K+-ATPase paralogs may contribute to population differences in salinity tolerance in a semi-anadromous fish. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 240, 110584. https://doi.org/10.1016/j.cbpa.2019.110584 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    21.Jeffries, K. M. et al. Divergent transcriptomic signatures in response to salinity exposure in two populations of an estuarine fish. Evol. Appl. 12, 1212–1226. https://doi.org/10.1111/eva.12799 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Lam, S. H. et al. Differential transcriptomic analyses revealed genes and signaling pathways involved in iono-osmoregulation and cellular remodeling in the gills of euryhaline Mozambique tilapia, Oreochromis mossambicus. BMC Genomics 15, 921. https://doi.org/10.1186/1471-2164-15-921 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Evans, T. G. & Kultz, D. The cellular stress response in fish exposed to salinity fluctuations. J. Exp. Zool. A Ecol. Integr. Physiol. 333, 421–435. https://doi.org/10.1002/jez.2350 (2020).Article 
    PubMed 

    Google Scholar 
    24.Burg, M. B., Ferraris, J. D. & Dmitrieva, N. I. Cellular response to hyperosmotic stresses. Physiol. Rev. 87, 1441–1474. https://doi.org/10.1152/physrev.00056.2006 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    25.Tine, M., Bonhomme, F., McKenzie, D. J. & Durand, J. D. Differential expression of the heat shock protein Hsp70 in natural populations of the tilapia, Sarotherodon melanotheron, acclimatised to a range of environmental salinities. BMC Ecol. 10, 11. https://doi.org/10.1186/1472-6785-10-11 (2010).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    26.Whitehead, A., Zhang, S., Roach, J. L. & Galvez, F. Common functional targets of adaptive micro- and macro-evolutionary divergence in killifish. Mol. Ecol. 22, 3780–3796. https://doi.org/10.1111/mec.12316 (2013).Article 
    PubMed 

    Google Scholar 
    27.Brennan, R. S., Galvez, F. & Whitehead, A. Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus. J. Exp. Biol. 218, 1212–1222. https://doi.org/10.1242/jeb.110445 (2015).Article 
    PubMed 

    Google Scholar 
    28.Kultz, D. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225–257. https://doi.org/10.1146/annurev.physiol.67.040403.103635 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    29.Takei, Y. & Hwang, P.-P. In Biology of Stress in Fish—Fish Physiology Vol. 35 (eds Schreck, C. B. et al.) 207–249 (Academic Press, 2016).Chapter 

    Google Scholar 
    30.Tseng, Y. C. & Hwang, P. P. Some insights into energy metabolism for osmoregulation in fish. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 148, 419–429. https://doi.org/10.1016/j.cbpc.2008.04.009 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    31.Chen, X. L., Lui, E. Y., Ip, Y. K. & Lam, S. H. RNA sequencing, de novo assembly and differential analysis of the gill transcriptome of freshwater climbing perch Anabas testudineus after 6 days of seawater exposure. J. Fish Biol. 93, 215–228. https://doi.org/10.1111/jfb.13653 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    32.Nguyen, T. V., Jung, H., Nguyen, T. M., Hurwood, D. & Mather, P. Evaluation of potential candidate genes involved in salinity tolerance in striped catfish (Pangasianodon hypophthalmus) using an RNA-Seq approach. Mar. Genomics 25, 75–88. https://doi.org/10.1016/j.margen.2015.11.010 (2016).Article 
    PubMed 

    Google Scholar 
    33.Bœuf, G. & Payan, P. How should salinity influence fish growth?. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130, 411–423. https://doi.org/10.1016/s1532-0456(01)00268-x (2001).Article 
    PubMed 

    Google Scholar 
    34.Makrinos, D. L. & Bowden, T. J. Natural environmental impacts on teleost immune function. Fish Shellfish Immunol. 53, 50–57. https://doi.org/10.1016/j.fsi.2016.03.008 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    35.Morgan, J. D. & Iwama, G. K. Effects of salinity on growth, metabolism, and ion regulation in juvenile rainbow and steelhead trout (Oncorhynchus mykiss) and fall chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci. 48, 2083–2094. https://doi.org/10.1139/f91-247 (1991).Article 

    Google Scholar 
    36.Whitehead, A., Roach, J. L., Zhang, S. & Galvez, F. Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient. Proc. Natl. Acad. Sci. U.S.A. 108, 6193–6198. https://doi.org/10.1073/pnas.1017542108 (2011).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    37.Kozak, G. M., Brennan, R. S., Berdan, E. L., Fuller, R. C. & Whitehead, A. Functional and population genomic divergence within and between two species of killifish adapted to different osmotic niches. Evolution 68, 63–80. https://doi.org/10.1111/evo.12265 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    38.Hrbek, T. & Meyer, A. Closing of the Tethys Sea and the phylogeny of Eurasian killifishes (Cyprinodontiformes: Cyprinodontidae). J. Evol. Biol. 16, 17–36. https://doi.org/10.1046/j.1420-9101.2003.00475.x (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    39.Schunter, C. et al. Desert fish populations tolerate extreme salinity change to overcome hydrological constraints. bioRxiv. https://doi.org/10.1101/2021.05.14.444120 (2021).Article 

    Google Scholar 
    40.Marshall, J. C. et al. Go with the flow: The movement behaviour of fish from isolated waterhole refugia during connecting flow events in an intermittent dryland river. Freshw. Biol. 61, 1242–1258. https://doi.org/10.1111/fwb.12707 (2016).Article 

    Google Scholar 
    41.Kerezsy, A., Balcombe, S. R., Tischler, M. & Arthington, A. H. Fish movement strategies in an ephemeral river in the Simpson Desert, Australia. Austral Ecol. 38, 798–808. https://doi.org/10.1111/aec.12075 (2013).Article 

    Google Scholar 
    42.Martin, C. H., Crawford, J. E., Turner, B. J. & Simons, L. H. Diabolical survival in Death Valley: Recent pupfish colonization, gene flow and genetic assimilation in the smallest species range on earth. Proc. Biol. Sci. 283, 20152334. https://doi.org/10.1098/rspb.2015.2334 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    43.Mossop, K. D. et al. Dispersal in the desert: Ephemeral water drives connectivity and phylogeography of an arid-adapted fish. J. Biogeogr. 42, 2374–2388. https://doi.org/10.1111/jbi.12596 (2015).Article 

    Google Scholar 
    44.Collins, J. P., Young, C., Howell, J. & Minckley, W. L. Impact of flooding in a Sonoran desert stream, including elimination of an endangered fish population (Poeciliopsis O. occidentalis, Poeciliidae). Southwest. Nat. 26, 415–423. https://doi.org/10.2307/3671085 (1981).Article 

    Google Scholar 
    45.Meffe, G. K. Effects of abiotic disturbance on coexistence of predator–prey fish species. Ecology 65, 1525–1534. https://doi.org/10.2307/1939132 (1984).Article 

    Google Scholar 
    46.Lotan, R. Sodium, chloride and water balance in the euryhaline teleost Aphanius dispar (Rüppell) (Cyprinodontidae). Z. Vgl. Physiol. 65, 455–462. https://doi.org/10.1007/bf00299054 (1969).Article 

    Google Scholar 
    47.Lotan, R. Osmotic adjustment in the euryhaline teleost Aphanius dispar (Cyprinodontidae). Z. Vgl. Physiol. 75, 383–387. https://doi.org/10.1007/bf00630558 (1971).CAS 
    Article 

    Google Scholar 
    48.Plaut, I. Resting metabolic rate, critical swimming speed, and routine activity of the euryhaline cyprinodontid, Aphanius dispar, acclimated to a wide range of salinities. Physiol. Biochem. Zool. 73, 590–596. https://doi.org/10.1086/317746 (2000).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    49.Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. https://doi.org/10.1093/bioinformatics/btu170 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    50.Andrews, S. FastQC: a quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/fastqc (2010).51.Song, L. & Florea, L. Rcorrector: Efficient and accurate error correction for Illumina RNA-seq reads. Gigascience 4, 48. https://doi.org/10.1186/s13742-015-0089-y (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Grabherr, M. G. et al. Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat. Biotechnol. 29, 644 (2011).CAS 
    Article 

    Google Scholar 
    53.Lafond-Lapalme, J., Duceppe, M. O., Wang, S., Moffett, P. & Mimee, B. A new method for decontamination of de novo transcriptomes using a hierarchical clustering algorithm. Bioinformatics 33, 1293–1300. https://doi.org/10.1093/bioinformatics/btw793 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    54.Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512. https://doi.org/10.1038/nprot.2013.084 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    55.Finn, R. D., Clements, J. & Eddy, S. R. HMMER web server: Interactive sequence similarity searching. Nucleic Acids Res. 39, W29–W37. https://doi.org/10.1093/nar/gkr367 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    56.Camacho, C. et al. BLAST+: Architecture and applications. BMC Bioinform. 10, 421. https://doi.org/10.1186/1471-2105-10-421 (2009).CAS 
    Article 

    Google Scholar 
    57.Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: Accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152. https://doi.org/10.1093/bioinformatics/bts565 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    58.Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. https://doi.org/10.1038/nmeth.1923 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    59.Simao, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212. https://doi.org/10.1093/bioinformatics/btv351 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    60.BioBam Bioinformatics. OmicsBox – Bioinformatics Made Easy. https://www.biobam.com/omicsbox (2019).61.Huerta-Cepas, J. et al. eggNOG 5.0: A hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309–D314. https://doi.org/10.1093/nar/gky1085 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    62.Gotz, S. et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 36, 3420–3435. https://doi.org/10.1093/nar/gkn176 (2008).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    63.Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419. https://doi.org/10.1038/nmeth.4197 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    64.Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. https://doi.org/10.1186/s13059-014-0550-8 (2014).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    65.Soneson, C., Love, M. I. & Robinson, M. D. Differential analyses for RNA-seq: Transcript-level estimates improve gene-level inferences. F1000Research https://doi.org/10.12688/f1000research.7563.1 (2015).Article 
    PubMed 

    Google Scholar 
    66.Zhu, A., Ibrahim, J. G. & Love, M. I. Heavy-tailed prior distributions for sequence count data: Removing the noise and preserving large differences. Bioinformatics 35, 2084–2092. https://doi.org/10.1093/bioinformatics/bty895 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    67.Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate—A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Stat. Methodol. 57, 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x (1995).MathSciNet 
    Article 
    MATH 

    Google Scholar 
    68.Cui, W. et al. Comparative transcriptomic analysis reveals mechanisms of divergence in osmotic regulation of the turbot Scophthalmus maximus. Fish Physiol. Biochem. 46, 1519–1536. https://doi.org/10.1007/s10695-020-00808-6 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    69.Lee, S. Y., Lee, H. J. & Kim, Y. K. Comparative transcriptome profiling of selected osmotic regulatory proteins in the gill during seawater acclimation of chum salmon (Oncorhynchus keta) fry. Sci. Rep. 10, 1987. https://doi.org/10.1038/s41598-020-58915-6 (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    70.Su, H., Ma, D., Zhu, H., Liu, Z. & Gao, F. Transcriptomic response to three osmotic stresses in gills of hybrid tilapia (Oreochromis mossambicus female × O. urolepis hornorum male). BMC Genomics 21, 110. https://doi.org/10.1186/s12864-020-6512-5 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    71.Fischer, D. S., Theis, F. J. & Yosef, N. Impulse model-based differential expression analysis of time course sequencing data. Nucleic Acids Res. 46, e119. https://doi.org/10.1093/nar/gky675 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    72.Hwang, P. P., Lee, T. H. & Lin, L. Y. Ion regulation in fish gills: Recent progress in the cellular and molecular mechanisms. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R28–R47. https://doi.org/10.1152/ajpregu.00047.2011 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    73.Marshall, W. S. Mechanosensitive signalling in fish gill and other ion transporting epithelia. Acta Physiol. (Oxf.) 202, 487–499. https://doi.org/10.1111/j.1748-1716.2010.02189.x (2011).CAS 
    Article 

    Google Scholar 
    74.Lema, S. C., Carvalho, P. G., Egelston, J. N., Kelly, J. T. & McCormick, S. D. Dynamics of gene expression responses for ion transport proteins and aquaporins in the gill of a euryhaline pupfish during freshwater and high-salinity acclimation. Physiol. Biochem. Zool. 91, 1148–1171. https://doi.org/10.1086/700432 (2018).Article 
    PubMed 

    Google Scholar 
    75.Flemmer, A. W. et al. Phosphorylation state of the Na+–K+–Cl− cotransporter (NKCC1) in the gills of Atlantic killifish (Fundulus heteroclitus) during acclimation to water of varying salinity. J. Exp. Biol. 213, 1558–1566. https://doi.org/10.1242/jeb.039644 (2010).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    76.Delpire, E. & Gagnon, K. B. SPAK and OSR1: STE20 kinases involved in the regulation of ion homoeostasis and volume control in mammalian cells. Biochem. J. 409, 321–331. https://doi.org/10.1042/BJ20071324 (2008).CAS 
    Article 
    PubMed 

    Google Scholar 
    77.Rinehart, J. et al. WNK2 kinase is a novel regulator of essential neuronal cation-chloride cotransporters. J. Biol. Chem. 286, 30171–30180. https://doi.org/10.1074/jbc.M111.222893 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    78.Li, J. et al. Gill transcriptomes reveal expression changes of genes related with immune and ion transport under salinity stress in silvery pomfret (Pampus argenteus). Fish Physiol. Biochem. 46, 1255–1277. https://doi.org/10.1007/s10695-020-00786-9 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    79.Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, R. D. & Somero, G. N. Living with water stress: Evolution of osmolyte systems. Science 217, 1214–1222. https://doi.org/10.1126/science.7112124 (1982).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    80.Kalujnaia, S., McVee, J., Kasciukovic, T., Stewart, A. J. & Cramb, G. A role for inositol monophosphatase 1 (IMPA1) in salinity adaptation in the euryhaline eel (Anguilla anguilla). FASEB J. 24, 3981–3991. https://doi.org/10.1096/fj.10-161000 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    81.Cui, W. X. et al. myo-inositol facilitates salinity tolerance by modulating multiple physiological functions in the turbot Scophthalmus maximus. Aquaculture 527, 735451. https://doi.org/10.1016/j.aquaculture.2020.735451 (2020).CAS 
    Article 

    Google Scholar 
    82.Ma, A. et al. Osmoregulation by the myo-inositol biosynthesis pathway in turbot Scophthalmus maximus and its regulation by anabolite and c-Myc. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 242, 110636. https://doi.org/10.1016/j.cbpa.2019.110636 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    83.Wang, Y. F., Yan, J. J., Tseng, Y. C., Chen, R. D. & Hwang, P. P. Molecular physiology of an extra-renal Cl− uptake mechanism for body fluid Cl− homeostasis. Int. J. Biol. Sci. 11, 1190–1203. https://doi.org/10.7150/ijbs.11737 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    84.Leguen, I., Le Cam, A., Montfort, J., Peron, S. & Fautrel, A. Transcriptomic analysis of trout gill ionocytes in fresh water and sea water using laser capture microdissection combined with microarray analysis. PLoS One 10, e0139938. https://doi.org/10.1371/journal.pone.0139938 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    85.Richards, J. G., Semple, J. W., Bystriansky, J. S. & Schulte, P. M. Na+/K+-ATPase alpha-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J. Exp. Biol. 206, 4475–4486. https://doi.org/10.1242/jeb.00701 (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    86.McCormick, S. D., Regish, A. M. & Christensen, A. K. Distinct freshwater and seawater isoforms of Na+/K+-ATPase in gill chloride cells of Atlantic salmon. J. Exp. Biol. 212, 3994–4001. https://doi.org/10.1242/jeb.037275 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    87.Bystriansky, J. S., Richards, J. G., Schulte, P. M. & Ballantyne, J. S. Reciprocal expression of gill Na+/K+-ATPase alpha-subunit isoforms alpha1a and alpha1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. J. Exp. Biol. 209, 1848–1858. https://doi.org/10.1242/jeb.02188 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    88.Tipsmark, C. K. et al. Switching of Na+, K+-ATPase isoforms by salinity and prolactin in the gill of a cichlid fish. J. Endocrinol. 209, 237–244. https://doi.org/10.1530/JOE-10-0495 (2011).CAS 
    Article 
    PubMed 

    Google Scholar 
    89.Urbina, M. A., Schulte, P. M., Bystriansky, J. S. & Glover, C. N. Differential expression of Na+, K+-ATPase alpha-1 isoforms during seawater acclimation in the amphidromous galaxiid fish Galaxias maculatus. J. Comp. Physiol. B 183, 345–357. https://doi.org/10.1007/s00360-012-0719-y (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    90.Velotta, J. P. et al. Transcriptomic imprints of adaptation to fresh water: Parallel evolution of osmoregulatory gene expression in the Alewife. Mol. Ecol. 26, 831–848. https://doi.org/10.1111/mec.13983 (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    91.Ip, Y. K. et al. Roles of three branchial Na+-K+-ATPase alpha-subunit isoforms in freshwater adaptation, seawater acclimation, and active ammonia excretion in Anabas testudineus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303, R112–R125. https://doi.org/10.1152/ajpregu.00618.2011 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    92.Birrer, S. C., Reusch, T. B. & Roth, O. Salinity change impairs pipefish immune defence. Fish Shellfish Immunol. 33, 1238–1248. https://doi.org/10.1016/j.fsi.2012.08.028 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    93.Delamare-Deboutteville, J., Wood, D. & Barnes, A. C. Response and function of cutaneous mucosal and serum antibodies in barramundi (Lates calcarifer) acclimated in seawater and freshwater. Fish Shellfish Immunol. 21, 92–101. https://doi.org/10.1016/j.fsi.2005.10.005 (2006).CAS 
    Article 
    PubMed 

    Google Scholar 
    94.Koppang, E. O., Kvellestad, A. & Fischer, U. In Mucosal Health in Aquaculture (eds Beck, B. H. & Peatman, E.) 93–133 (Academic Press, 2015).Chapter 

    Google Scholar 
    95.Poulin, R., Blanar, C. A., Thieltges, D. W. & Marcogliese, D. J. The biogeography of parasitism in sticklebacks: Distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34, 540–551. https://doi.org/10.1111/j.1600-0587.2010.06826.x (2011).Article 

    Google Scholar 
    96.Takemura, A. F., Chien, D. M. & Polz, M. F. Associations and dynamics of Vibrionaceae in the environment, from the genus to the population level. Front. Microbiol. 5, 38. https://doi.org/10.3389/fmicb.2014.00038 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    97.Nitzan, S., Shwartsburd, B. & Heller, E. D. The effect of growth medium salinity of Photobacterium damselae subsp. piscicida on the immune response of hybrid bass (Morone saxatilis × M. chrysops). Fish Shellfish Immunol. 16, 107–116. https://doi.org/10.1016/s1050-4648(03)00045-7 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    98.Zheng, D. H. et al. Effect of temperature and salinity on virulence of Edwardsiella tarda to Japanese flounder, Paralichthys olivaceus (Temminck et Schlegel). Aquac. Res. 35, 494–500. https://doi.org/10.1111/j.1365-2109.2004.01044.x (2004).Article 

    Google Scholar 
    99.Dominguez, M., Takemura, A., Tsuchiya, M. & Nakamura, S. Impact of different environmental factors on the circulating immunoglobulin levels in the Nile tilapia, Oreochromis niloticus. Aquaculture 241, 491–500. https://doi.org/10.1016/j.aquaculture.2004.06.027 (2004).CAS 
    Article 

    Google Scholar 
    100.Mozanzadeh, M. T. et al. The effect of salinity on growth performance, digestive and antioxidant enzymes, humoral immunity and stress indices in two euryhaline fish species: Yellowfin seabream (Acanthopagrus latus) and Asian seabass (Lates calcarifer). Aquaculture 534, 736329. https://doi.org/10.1016/j.aquaculture.2020.736329 (2021).CAS 
    Article 

    Google Scholar 
    101.Gao, Y., Tang, X., Sheng, X., Xing, J. & Zhan, W. Antigen uptake and expression of antigen presentation-related immune genes in flounder (Paralichthys olivaceus) after vaccination with an inactivated Edwardsiella tarda immersion vaccine, following hyperosmotic treatment. Fish Shellfish Immunol. 55, 274–280. https://doi.org/10.1016/j.fsi.2016.05.042 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    102.Salinas, I. The mucosal immune system of teleost fish. Biology 4, 525–539. https://doi.org/10.3390/biology4030525 (2015).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    103.Reverter, M., Tapissier-Bontemps, N., Lecchini, D., Banaigs, B. & Sasal, P. Biological and ecological roles of external fish mucus: A review. Fishes 3, 41. https://doi.org/10.3390/fishes3040041 (2018).Article 

    Google Scholar 
    104.Shephard, K. L. Functions for fish mucus. Rev. Fish Biol. Fish. 4, 401–429. https://doi.org/10.1007/Bf00042888 (1994).Article 

    Google Scholar 
    105.Wong, M. K. S. et al. A sodium binding system alleviates acute salt stress during seawater acclimation in eels. Zool. Lett. 3, 22. https://doi.org/10.1186/s40851-017-0081-8 (2017).Article 

    Google Scholar 
    106.Malachowicz, M., Wenne, R. & Burzynski, A. De novo assembly of the sea trout (Salmo trutta m. trutta) skin transcriptome to identify putative genes involved in the immune response and epidermal mucus secretion. PLoS One 12, e0172282. https://doi.org/10.1371/journal.pone.0172282 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    107.Roberts, S. D. & Powell, M. D. Comparative ionic flux and gill mucous cell histochemistry: Effects of salinity and disease status in Atlantic salmon (Salmo salar L.). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 134, 525–537. https://doi.org/10.1016/s1095-6433(02)00327-6 (2003).Article 
    PubMed 

    Google Scholar 
    108.Mylonas, C. C. et al. Growth performance and osmoregulation in the shi drum (Umbrina cirrosa) adapted to different environmental salinities. Aquaculture 287, 203–210. https://doi.org/10.1016/j.aquaculture.2008.10.024 (2009).CAS 
    Article 

    Google Scholar 
    109.Roberts, S. D. & Powell, M. D. The viscosity and glycoprotein biochemistry of salmonid mucus varies with species, salinity and the presence of amoebic gill disease. J. Comp. Physiol. B 175, 1–11. https://doi.org/10.1007/s00360-004-0453-1 (2005).CAS 
    Article 
    PubMed 

    Google Scholar 
    110.Kalujnaia, S. et al. Transcriptomic approach to the study of osmoregulation in the European eel Anguilla anguilla. Physiol. Genomics 31, 385–401. https://doi.org/10.1152/physiolgenomics.00059.2007 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    111.Shaw, J. R. et al. The role of SGK and CFTR in acute adaptation to seawater in Fundulus heteroclitus. Cell Physiol. Biochem. 22, 69–78. https://doi.org/10.1159/000149784 (2008).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    112.Kammerer, B. D., Sardella, B. A. & Kultz, D. Salinity stress results in rapid cell cycle changes of tilapia (Oreochromis mossambicus) gill epithelial cells. J. Exp. Zool. A Ecol. Genet. Physiol. 311, 80–90. https://doi.org/10.1002/jez.498 (2009).Article 
    PubMed 

    Google Scholar 
    113.Ronkin, D., Seroussi, E., Nitzan, T., Doron-Faigenboim, A. & Cnaani, A. Intestinal transcriptome analysis revealed differential salinity adaptation between two tilapiine species. Comp. Biochem. Physiol. Part D Genomics Proteomics 13, 35–43. https://doi.org/10.1016/j.cbd.2015.01.003 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    114.Dong, Y. W. et al. Genomic and physiological mechanisms underlying skin plasticity during water to air transition in an amphibious fish. J. Exp. Biol. 224, jeb235515. https://doi.org/10.1242/jeb.235515 (2021).Article 
    PubMed 

    Google Scholar 
    115.Inokuchi, M. & Kaneko, T. Recruitment and degeneration of mitochondrion-rich cells in the gills of Mozambique tilapia Oreochromis mossambicus during adaptation to a hyperosmotic environment. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 162, 245–251. https://doi.org/10.1016/j.cbpa.2012.03.018 (2012).CAS 
    Article 
    PubMed 

    Google Scholar  More

  • in

    Selection of mesophotic habitats by Oculina patagonica in the Eastern Mediterranean Sea following global warming

    1.Cook, B. I., Wolkovich, E. M. & Parmesan, C. Divergent responses to spring and winter warming drive community level flowering trends. Proc. Natl. Acad. Sci. USA 109, 9000–9005 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Chen, I. C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science (80-). 333, 1024–1026 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    3.Suggitt, A. J. et al. Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8 (2011).Article 

    Google Scholar 
    4.Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Change 3, 919–925 (2013).ADS 
    Article 

    Google Scholar 
    5.Suggitt, A. J., et al. Habitatmicroclimates drive fine-scale variation in extreme temperatures. Oikos 120, 1–8. https://doi.org/10.1111/j.1600-0706.2010.18270.x (2011).Article 

    Google Scholar 
    6.Kersting, D. K., Bensoussan, N. & Linares, C. Long-term responses of the endemic reef-builder cladocora caespitosa to mediterranean warming. PLoS ONE 8, e70820 (2013).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Rodolfo-Metalpa, R. et al. Thermally tolerant corals have limited capacity to acclimatize to future warming. Glob. Change Biol. 20, 3036–3049 (2014).ADS 
    Article 

    Google Scholar 
    8.Fine M., & Loya Y. Coral bleaching in a temperate sea: From colony physiology to population ecology. In: Coral Health and Disease (eds. Rosenberg, E., & Loya, Y). https://doi.org/10.1007/978-3-662-06414-6_6 (Springer, Berlin, Heidelberg 2004).9.Liu, G., Strong, A. E., Skirving, W. J. & Arzayus, L. F. Overview of NOAA Coral Reef Watch Program’s near-real-time satellite global coral bleaching monitoring activities. Proc. 10th Int. Coral Reef Symp. 1793, 1783–1793 (2006).
    Google Scholar 
    10.Glynn, P. W. Coral reef bleaching: Facts, hypotheses and implications. Glob. Change Biol. 2, 495–509 (1996).ADS 
    Article 

    Google Scholar 
    11.Price, N. N. et al. Global biogeography of coral recruitment: Tropical decline and subtropical increase. Mar. Ecol. Prog. Ser. 621, 1–17 (2019).ADS 
    Article 

    Google Scholar 
    12.Serrano, E. et al. Rapid northward spread of a zooxanthellate coral enhanced by artificial structures and sea warming in the Western Mediterranean. PLoS One 8(1), e52739. https://doi.org/10.1371/journal.pone.0052739 (2013).CAS 
    Article 

    Google Scholar 
    13.Grupstra, C. G. B. et al. Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes. Coral Reefs 2017 363. 36, 981–985 (2017).
    Google Scholar 
    14.Serrano, E., Ribes, M. & Coma, R. Demographics of the zooxanthellate coral Oculina patagonica along the Mediterranean Iberian coast in relation to environmental parameters. Sci. Total Environ. 634, 1580–1592 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    15.Leichter, J. J., Helmuth, B. & Fischer, A. M. Variation beneath the surface: Quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida. J. Mar. Res. 64, 563–588 (2006).Article 

    Google Scholar 
    16.Gould, K., Bruno, J. F., Ju, R. & Goodbody-Gringley, G. Upper-mesophotic and shallow reef corals exhibit similar thermal tolerance, sensitivity and optima. Coral Reefs https://doi.org/10.1007/s00338-021-02095-w (2021).Article 

    Google Scholar 
    17.Semmler, R. F., Hoot, W. C. & Reaka, M. L. Are mesophotic coral ecosystems distinct communities and can they serve as refugia for shallow reefs?. Coral Reefs 36, 433–444 (2017).ADS 
    Article 

    Google Scholar 
    18.Shlesinger, T. & Loya, Y. Depth-dependent parental effects create invisible barriers to coral dispersal. Commun. Biol. 4(202), https://doi.org/10.1038/s42003-021-01727-9 (2021).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    19.Ledoux, J.-B. et al. Potential for adaptive evolution at species range margins: Contrasting interactions between red coral populations and their environment in a changing ocean. Ecol. Evol. 5, 1178–1192 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Liberman, R., Shlesinger, T., Loya, Y. & Benayahu, Y. Octocoral sexual reproduction: Temporal disparity between mesophotic and shallow-reef populations. Front. Mar. Sci. 5, 1–14 (2018).Article 

    Google Scholar 
    21.Rapuano, H., Shlesinger, T., Loya, Y., Amit, T. & Grinblat, M. Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt. Ecology 99, 421–437 (2017).
    Google Scholar 
    22.Bongaerts, P., Ridgway, T., Sampayo, E. M. & Hoegh-Guldberg, O. Assessing the ‘deep reef refugia’ hypothesis: Focus on Caribbean reefs. Coral Reefs 29, 1–19 (2010).Article 

    Google Scholar 
    23.Hoogenboom, M., Rodolfo-Metalpa, R. & Ferrier-Pagès, C. Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J. Exp. Biol. 213, 2399–2409 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    24.Mass, T. et al. Photoacclimation of Stylophora pistillata to light extremes: Metabolism and calcification. Mar. Ecol. Prog. Ser. 334, 93–102 (2007).ADS 
    CAS 
    Article 

    Google Scholar 
    25.Bednarz, V. N., Grover, R., Maguer, J. F., Fine, M. & Ferrier-Pagès, C. The assimilation of diazotroph-derived nitrogen by scleractinian corals depends on their metabolic status. MBio 8, e02058-16 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Grottoli, A. G., Rodrigues, L. J. & Palardy, J. E. Heterotrophic plasticity and resilience in bleached corals. Nature 440, 1186–1189 (2006).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Tremblay, P. et al. Controlling effects of irradiance and heterotrophy on carbon translocation in the temperate coral Cladocora caespitosa. PLoS ONE 7, e44672 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Aichelman, H. E., Zimmerman, R. C. & Barshis, D. J. Adaptive signatures in thermal performance of the temperate coral Astrangia poculata. J. Exp. Biol. 222, jeb189225 (2019).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    29.Shenkar, N., Fine, M. & Loya, Y. Size matters: Bleaching dynamics of the coral Oculina patagonica. Mar. Ecol. Prog. Ser. 294, 181–188 (2005).ADS 
    Article 

    Google Scholar 
    30.Zaquin, T., Zaslansky, P., Pinkas, I. & Mass, T. Simulating bleaching: Long-term adaptation to the dark reveals phenotypic plasticity of the Mediterranean Sea coral Oculina patagonica. Front. Mar. Sci. 6, 662 https://doi.org/10.3389/fmars.2019.00662 (2019).Article 

    Google Scholar 
    31.De Angelis d’Ossat, G. Altri Zoantari del Terziario della Patagonia. (1908).32.Fine, M. & Loya, Y. The coral Oculina patagonica a new immigrant to the Mediterranean coast of Israel. Isr. J. Zool. 41, 84 (1995).
    Google Scholar 
    33.Salomidi, M., Katsanevakis, S., Issaris, Y., Tsiamis, K. & Katsiaras, N. Anthropogenic disturbance of coastal habitats promotes the spread of the introduced scleractinian coral Oculina patagonica in the Mediterranean Sea. Biol. Invasions 15, 1961–1971 (2013).Article 

    Google Scholar 
    34.Fine, M., Zibrowius, H. & Loya, Y. Oculina patagonica: A non-lessepsian scleractinian coral invading the Mediterranean Sea. Mar. Biol. 138, 1195–1203 (2001).Article 

    Google Scholar 
    35.Sartoretto, S. et al. The alien coral Oculina patagonica De Angelis, 1908 (Cnidaria, Scleractinia) in Algeria and Tunisia. Aquat. Invasions 3, 173–180 (2008).Article 

    Google Scholar 
    36.Ozer, T., Gertman, I., Kress, N., Silverman, J. & Herut, B. Interannual thermohaline (1979–2014) and nutrient (2002–2014) dynamics in the Levantine surface and intermediate water masses, SE Mediterranean Sea. Glob. Planet. Change 151, 60–67 (2017).ADS 
    Article 

    Google Scholar 
    37.Leydet, K. P. & Hellberg, M. E. The invasive coral Oculina patagonica has not been recently introduced to the Mediterranean from the western Atlantic. BMC Evol. Biol. 15(79), https://doi.org/10.1186/s12862-015-0356-7 (2015).38.Veron, J. E. N. Título: Corals of the world. P.imprenta: Australia. Australian Institute of Marine Science. 463, 31 (2000).39.Einbinder, S. et al. Changes in morphology and diet of the coral Stylophora pistillata along a depth gradient. Mar. Ecol. Prog. Ser. 381, 167–174 (2009).ADS 
    Article 

    Google Scholar 
    40.Goodbody-Gringley, G. & Waletich, J. Morphological plasticity of the depth generalist coral, Montastraea cavernosa, on mesophotic reefs in Bermuda. Ecology 99, 1688–1690 (2018).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    41.Malik, A. et al. Molecular and skeletal fingerprints of scleractinian coral biomineralization: From the sea surface to mesophotic depths. Acta Biomater. https://doi.org/10.1016/j.actbio.2020.01.010 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Frade, P. R., Englebert, N., Faria, J., Visser, P. M. & Bak, R. P. M. Distribution and photobiology of Symbiodinium types in different light environments for three colour morphs of the coral Madracis pharensis: Is there more to it than total irradiance?. Coral Reefs 27, 913–925 (2008).ADS 
    Article 

    Google Scholar 
    43.Lesser, M. P. et al. Photoacclimatization by the coral Montastraea cavernosa in the mesophotic zone: Light, food, and genetics. Ecology 91, 990–1003 (2010).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    44.Byler, K. A., Carmi-Veal, M., Fine, M. & Goulet, T. L. Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. PLoS ONE 8, 1–7 (2013).Article 
    CAS 

    Google Scholar 
    45.Scucchia, F., Nativ, H., Neder, M., Goodbody-Gringley, G. & Mass, T. Physiological characteristics of Stylophora pistillata larvae across a depth gradient. Front. Mar. Sci. https://doi.org/10.3389/fmars.2020.00013 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    46.Leydet, K. P. & Hellberg, M. E. Discordant coral–symbiont structuring: factors shaping geographical variation of Symbiodinium communities in a facultative zooxanthellate coral genus, Oculina. Coral Reefs 35, 583–595 (2016).ADS 
    Article 

    Google Scholar 
    47.Rubio-Portillo, E. et al. Eukarya associated with the stony coral Oculina patagonica from the Mediterranean Sea. Mar. Genom. 17, 17–23 (2014).Article 

    Google Scholar 
    48.Brakel, W. H. Small-scale spatial variation in light available to coral reef benthos: Quantum irradiance measurements from a Jamaican reef. Bull. Mar. Sci. 29, 406–413 (1979).ADS 

    Google Scholar 
    49.Ben-Zvi, O. et al. Photophysiology of a mesophotic coral 3 years after transplantation to a shallow environment. Coral Reefs 39, 903–913 (2020).Article 

    Google Scholar 
    50.Wang, C., Arneson, E. M., Gleason, D. F. & Hopkinson, B. M. Resilience of the temperate coral Oculina arbuscula to ocean acidification extends to the physiological level. Coral Reefs 40, 201–214 (2021).Article 

    Google Scholar 
    51.Hoogenboom, M., Béraud, E. & Ferrier-Pagès, C. Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29, 21–29. https://doi.org/10.1007/s00338-009-0558-9 (2010).ADS 
    Article 

    Google Scholar 
    52.Martinez, S. et al. Effect of different derivatization protocols on the calculation of trophic position using amino acids compound-specific stable isotopes. Front. Mar. Sci. 7, 1–7. https://doi.org/10.3389/fmars.2020.561568 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    53.Wall, C. B., Wallsgrove, N. J., Gates, R. D. & Popp, B. N. Amino acid δ 13C and δ 15N analyses reveal distinct species‐specific patterns of trophic plasticity in a marine symbiosis. Limnol. Oceanogr. 66, 2033–2050. https://doi.org/10.1002/lno.11742 (2021).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    54.Ferrier-Pagès, C. et al. Tracing the trophic plasticity of the coral-dinoflagellate symbiosis using amino acid compound-specific stable isotope analysis. Microorganisms 9, 1–16 (2021).Article 

    Google Scholar 
    55.Grossowicz, M., Shemesh, E., Martinez, S., Benayahu, Y. & Tchernov, D. New evidence of Melithaea erythraea colonization in the Mediterranean. Estuar. Coast. Shelf Sci. 236, 106652 (2020).Article 

    Google Scholar 
    56.Leal, M. C. et al. Trophic ecology of the facultative symbiotic coral Oculina arbuscula. Mar. Ecol. Prog. Ser. 504, 171–179 (2014).ADS 
    Article 

    Google Scholar 
    57.Ferrier-Pagès, C. et al. Summer autotrophy and winter heterotrophy in the temperate symbiotic coral Cladocora caespitosa. Limnol. Oceanogr. 56, 1429–1438 (2011).ADS 
    Article 

    Google Scholar 
    58.Ezzat, L., Fine, M., Maguer, J.-F., Grover, R. & Ferrier-Pagès, C. Carbon and nitrogen acquisition in shallow and deep holobionts of the Scleractinian coral S. pistillata. Front. Mar. Sci. 4, 1–12. https://doi.org/10.3389/fmars.2017.00102 (2017).Article 

    Google Scholar 
    59.Martinez, S. et al. Energy sources of the depth-generalist mixotrophic coral Stylophora pistillata. Front. Mar. Sci. 7, 1–16 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    60.Wall, C. B., Kaluhiokalani, M., Popp, B. N., Donahue, M. J. & Gates, R. D. Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient. ISME J. 14, 945–958 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Fox, M. D., Elliott Smith, E. A., Smith, J. E. & Newsome, S. D. Trophic plasticity in a common reef-building coral: Insights from δ13C analysis of essential amino acids. Funct. Ecol. 33, 2203–2214 (2019).Article 

    Google Scholar 
    62.Godinot, C., Grover, R., Allemand, D. & Ferrier-Pagès, C. High phosphate uptake requirements of the scleractinian coral Stylophora pistillata. J. Exp. Biol. 214, 2749–2754 (2011).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    63.Kersting, D. K. et al. Experimental evidence of the synergistic effects of warming and invasive algae on a temperate reef-builder coral. Sci. Rep. 2015 51 5, 1–8 (2015).
    Google Scholar 
    64.Suari, Y. et al. A long term physical and biogeochemical database of a hyper-eutrophicated Mediterranean micro-estuary. Data Br. 27, 104809 (2019).Article 

    Google Scholar 
    65.Liberman, R., Fine, M. & Benayahu, Y. Simulated climate change scenarios impact the reproduction and early life stages of a soft coral. Mar. Environ. Res. 163, 105215. https://doi.org/10.1016/j.marenvres.2020.105215 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    66.Jeffrey, S. W. & Humphrey, G. F. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pflanz. 167, 191–194 (1975).CAS 
    Article 

    Google Scholar 
    67.Marsh, J. A. Primary productivity of reef-building calcareous red algae. Ecology 51, 255–263 (1970).Article 

    Google Scholar 
    68.Chisholm, J. R. M. & Gattuso, J.-P. Validation of the alkalinity anomaly technique for investigating calcification of photosynthesis in coral reef communities. Limnol. Oceanogr. 36, 1232–1239 (1991).ADS 
    CAS 
    Article 

    Google Scholar 
    69.Schneider, K. & Erez, J. The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol. Oceanogr. 51, 1284–1293 (2006).ADS 
    CAS 
    Article 

    Google Scholar 
    70.Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. DNA primers for amplification of mitochondrial Cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    71.Arif, C. et al. Assessing Symbiodinium diversity in scleractinian corals via next-generation sequencing-based genotyping of the ITS2 rDNA region. Mol. Ecol. 23, 4418–4433 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    73.Hume, B. C. C. et al. SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol. Ecol. Resour. 19, 1063–1080 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Grover, R., Maguer, J.-F., Reynaud-Vaganay, S. & Ferrier-Pagès, C. Uptake of ammonium by the scleractinian coral Stylophora pistillata : Effect of feeding, light, and ammonium concentrations. Limnol. Oceanogr. 47, 782–790 (2002).ADS 
    Article 

    Google Scholar 
    75.Tremblay, P., Grover, R., Maguer, J. F., Legendre, L. & Ferrier-Pagès, C. Autotrophic carbon budget in coral tissue: A new 13C-based model of photosynthate translocation. J. Exp. Biol. 215, 1384–1393 (2012).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    76.Cowie, G. L. & Hedges, J. I. Improved amino acid quantification in environmental samples: Charge-matched recovery standards and reduced analysis time. Mar. Chem. 37, 223–238 (1992).CAS 
    Article 

    Google Scholar 
    77.Docherty, G., Jones, V. & Evershed, R. P. Practical and theoretical considerations in the gas chromatography/combustion/isotope ratio mass spectrometry δ 13C analysis of small polyfunctional compounds. Rapid Commun. Mass Spectrom. 15, 730–738 (2001).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    78.R Core Team. R: A Language and Environment for Statistical Computing. (2020).79.Fox, J. W., & Weisberg, S. An R companion to applied regression. 3rd ed. (Los Angeles: SAGE Publications, Inc, 2019)
    Google Scholar 
    80.Villanueva, R. A. M. & Chen, Z. J. ggplot2: Elegant graphics for data analysis (2nd ed.), Measurement: Interdisciplinary Research and Perspectives, 17(3), 160–167. https://doi.org/10.1080/15366367.2019.1565254 (2019).81.Wilke, C. O. cowplot: Streamlined Plot Theme and Plot Annotations for “ggplot2” (R 74 package version 1.1.0) [Computer software]. https://CRAN.Rproject.org/package=cowplot (2020). More

  • in

    Non-diphtheriae Corynebacterium species are associated with decreased risk of pneumococcal colonization during infancy

    1.Backhaus E, Berg S, Andersson R, Ockborn G, Malmström P, Dahl M, et al. Epidemiology of invasive pneumococcal infections: manifestations, incidence and case fatality rate correlated to age, gender and risk factors. BMC Infect Dis. 2016;16:367.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    2.Bogaert D, de Groot R, Hermans P. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis. 2004;4:144–54.PubMed 
    Article 
    CAS 

    Google Scholar 
    3.Wahl B, O’Brien KL, Greenbaum A, Majumder A, Liu L, Chu Y, et al. Burden of Streptococcus pneumoniae and Haemophilus influenzae type b disease in children in the era of conjugate vaccines: global, regional, and national estimates for 2000-15. Lancet Glob Health. 2018;6:e744–57.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    4.McAllister DA, Liu L, Shi T, Chu Y, Reed C, Burrows J, et al. Global, regional, and national estimates of pneumonia morbidity and mortality in children younger than 5 years between 2000 and 2015: a systematic analysis. Lancet Glob Health. 2019;7:e47–57.PubMed 
    Article 

    Google Scholar 
    5.Abdullahi O, Karani A, Tigoi CC, Mugo D, Kungu S, Wanjiru E, et al. The prevalence and risk factors for pneumococcal colonization of the nasopharynx among children in Kilifi District, Kenya. PloS ONE. 2012;7:e30787.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    6.Kelly MS, Surette MG, Smieja M, Rossi L, Luinstra K, Steenhoff AP, et al. Pneumococcal colonization and the nasopharyngeal microbiota of children in Botswana. Pediatr Infect Dis J. 2018;37:1176–83.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Huang SS, Hinrichsen VL, Stevenson AE, Rifas-Shiman SL, Kleinman K, Pelton SI, et al. Continued impact of pneumococcal conjugate vaccine on carriage in young children. Pediatrics 2009;124:e1–e11.PubMed 
    Article 

    Google Scholar 
    8.van Hoek AJ, Sheppard CL, Andrews NJ, Waight PA, Slack MP, Harrison TG, et al. Pneumococcal carriage in children and adults two years after introduction of the thirteen valent pneumococcal conjugate vaccine in England. Vaccine.2014;32:4349–55.PubMed 
    Article 

    Google Scholar 
    9.Almeida ST, Nunes S, Paulo ACS, Valadares I, Martins S, Breia F, et al. Low prevalence of pneumococcal carriage and high serotype and genotype diversity among adults over 60 years of age living in Portugal. PloS ONE 2014;9:e90974.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    10.Kaplan SL, Mason EO, Wald ER, Schutze GE, Bradley JS, Tan TQ, et al. Decrease of invasive pneumococcal infections in children among 8 children’s hospitals in the United States after the introduction of the 7-valent pneumococcal conjugate vaccine. Pediatrics.2004;113:443–9.PubMed 
    Article 

    Google Scholar 
    11.Hammitt LL, Etyang AO, Morpeth SC, Ojal J, Mutuku A, Mturi N, et al. Effect of ten-valent pneumococcal conjugate vaccine on invasive pneumococcal disease and nasopharyngeal carriage in Kenya: a longitudinal surveillance study. Lancet.2019;393:2146–54.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    12.Cutts F, Zaman S, Enwere GY, Jaffar S, Levine O, Okoko J, et al. Efficacy of nine-valent pneumococcal conjugate vaccine against pneumonia and invasive pneumococcal disease in The Gambia: randomised, double-blind, placebo-controlled trial. Lancet.2005;365:1139–46.PubMed 
    Article 
    CAS 

    Google Scholar 
    13.Congdon M, Hong H, Young RR, Cunningham CK, Enane LA, Arscott-Mills T, et al. Effect of Haemophilus influenzae type b and 13-valent pneumococcal conjugate vaccines on childhood pneumonia hospitalizations and deaths in Botswana. Clin Infect Dis. 2020; e-pub ahead of print 8 July 2020; https://doi.org/10.1093/cid/ciaa919.14.Eskola J, Kilpi T, Palmu A, Jokinen J, Eerola M, Haapakoski J, et al. Efficacy of a pneumococcal conjugate vaccine against acute otitis media. N. Engl J Med. 2001;344:403–9.PubMed 
    Article 
    CAS 

    Google Scholar 
    15.Pelton SI, Huot H, Finkelstein JA, Bishop CJ, Hsu KK, Kellenberg J, et al. Emergence of 19A as virulent and multidrug resistant Pneumococcus in Massachusetts following universal immunization of infants with pneumococcal conjugate vaccine. Pediatr Infect Dis J. 2007;26:468–72.PubMed 
    Article 

    Google Scholar 
    16.Pichichero ME, Casey JR. Emergence of a multiresistant serotype 19A pneumococcal strain not included in the 7-valent conjugate vaccine as an otopathogen in children. JAMA.2007;298:1772–8.PubMed 
    Article 
    CAS 

    Google Scholar 
    17.Neves FP, Cardoso NT, Snyder RE, Marlow MA, Cardoso CA, Teixeira LM, et al. Pneumococcal carriage among children after four years of routine 10-valent pneumococcal conjugate vaccine use in Brazil: the emergence of multidrug resistant serotype 6C. Vaccine.2017;35:2794–800.PubMed 
    Article 

    Google Scholar 
    18.Bradshaw JL, McDaniel LS. Selective pressure: rise of the nonencapsulated pneumococcus. PLoS Pathog. 2019;15:e1007911.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    19.Ladhani SN, Collins S, Djennad A, Sheppard CL, Borrow R, Fry NK, et al. Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000–17: a prospective national observational cohort study. Lancet Infect Dis. 2018;18:441–51.PubMed 
    Article 

    Google Scholar 
    20.Ouldali N, Levy C, Varon E, Bonacorsi S, Béchet S, Cohen R, et al. Incidence of paediatric pneumococcal meningitis and emergence of new serotypes: a time-series analysis of a 16-year French national survey. Lancet Infect Dis. 2018;18:983–91.PubMed 
    Article 

    Google Scholar 
    21.Zaneveld J, Turnbaugh PJ, Lozupone C, Ley RE, Hamady M, Gordon JI, et al. Host-bacterial coevolution and the search for new drug targets. Curr Opin Chem Biol. 2008;12:109–14.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    22.de Steenhuijsen Piters WA, Binkowska J, Bogaert D. Early life microbiota and respiratory tract infections. Cell Host Microbe. 2020;28:223–32.PubMed 
    Article 
    CAS 

    Google Scholar 
    23.Bogaert D, van Belkum A, Sluijter M, Luijendijk A, de Groot R, Rümke H, et al. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet.2004;363:1871–2.PubMed 
    Article 
    CAS 

    Google Scholar 
    24.Pettigrew MM, Gent JF, Revai K, Patel JA, Chonmaitree T. Microbial interactions during upper respiratory tract infections. Emerg Infect Dis. 2008;14:1584.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Shiri T, Nunes MC, Adrian PV, Van Niekerk N, Klugman KP, Madhi SA. Interrelationship of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus colonization within and between pneumococcal-vaccine naïve mother–child dyads. BMC Infect Dis. 2013;13:483.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Jacoby P, Watson K, Bowman J, Taylor A, Riley TV, Smith DW, et al. Modelling the co-occurrence of Streptococcus pneumoniae with other bacterial and viral pathogens in the upper respiratory tract. Vaccine.2007;25:2458–64.PubMed 
    Article 

    Google Scholar 
    27.Nzenze S, Shiri T, Nunes M, Klugman K, Kahn K, Twine R, et al. Temporal association of infant immunisation with pneumococcal conjugate vaccine on the ecology of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus nasopharyngeal colonisation in a rural South African community. Vaccine.2014;32:5520–30.PubMed 
    Article 
    CAS 

    Google Scholar 
    28.Faden H, Stanievich J, Brodsky L, Bernstein J, Ogra PL. Changes in nasopharyngeal flora during otitis media of childhood. Pediatr Infect Dis J. 1990;9:623–6.PubMed 
    CAS 

    Google Scholar 
    29.Shekhar S, Khan R, Schenck K, Petersen FC. Intranasal Immunization with the commensal Streptococcus mitis confers protective immunity against pneumococcal lung infection. Appl Environ Microbiol. 2019;85:e02235–18.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    30.Cangemi de Gutierrez R, Santos V, Nader-Macias ME. Protective effect of intranasally inoculated Lactobacillus fermentum against Streptococcus pneumoniae challenge on the mouse respiratory tract. FEMS Immunol Med Microbiol. 2001;31:187–95.PubMed 
    Article 
    CAS 

    Google Scholar 
    31.Wong SS, Quan Toh Z, Dunne EM, Mulholland EK, Tang ML, Robins-Browne RM, et al. Inhibition of Streptococcus pneumoniae adherence to human epithelial cells in vitro by the probiotic Lactobacillus rhamnosus GG. BMC Res Notes. 2013;6:135.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Laufer AS, Metlay JP, Gent JF, Fennie KP, Kong Y, Pettigrew MM. Microbial communities of the upper respiratory tract and otitis media in children. mBio.2011;2:e00245–10.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Bomar L, Brugger SD, Yost BH, Davies SS, Lemon KP. Corynebacterium accolens releases antipneumococcal free fatty acids from human nostril and skin surface triacylglycerols. mBio.2016;7:e01725–15.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    34.Cope EK, Goldstein-Daruech N, Kofonow JM, Christensen L, McDermott B, Monroy F, et al. Regulation of virulence gene expression resulting from Streptococcus pneumoniae and nontypeable Haemophilus influenzae interactions in chronic disease. PloS ONE. 2011;6:e28523.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    35.Lysenko ES, Ratner AJ, Nelson AL, Weiser JN. The role of innate immune responses in the outcome of interspecies competition for colonization of mucosal surfaces. PloS Pathog. 2005;1:e1.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    36.Weimer KE, Juneau RA, Murrah KA, Pang B, Armbruster CE, Richardson SH, et al. Divergent mechanisms for passive pneumococcal resistance to β-lactam antibiotics in the presence of Haemophilus influenzae. J Infect Dis. 2011;203:549–55.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    37.Tikhomirova A, Kidd SP. Haemophilus influenzae and Streptococcus pneumoniae: living together in a biofilm. Pathog Dis. 2013;69:114–26.PubMed 
    Article 
    CAS 

    Google Scholar 
    38.Brugger SD, Eslami SM, Pettigrew MM, Escapa IF, Henke MT, Kong Y, et al. Dolosigranulum pigrum cooperation and competition in human nasal microbiota. mSphere. 2020;5.39.Teo SM, Mok D, Pham K, Kusel M, Serralha M, Troy N, et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe. 2015;17:704–15.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    40.Mika M, Mack I, Korten I, Qi W, Aebi S, Frey U, et al. Dynamics of the nasal microbiota in infancy: a prospective cohort study. J Allergy Clin Immunol. 2015;135:905–12.PubMed 
    Article 

    Google Scholar 
    41.Biesbroek G, Tsivtsivadze E, Sanders EA, Montijn R, Veenhoven RH, Keijser BJ, et al. Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am J Respir Crit Care Med. 2014;190:1283–92.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    42.Bosch AA, Levin E, van Houten MA, Hasrat R, Kalkman G, Biesbroek G, et al. Development of upper respiratory tract microbiota in infancy is affected by mode of delivery. EBioMedicine.2016;9:336–45.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA. 2010;107:11971–5.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Biesbroek G, Bosch AA, Wang X, Keijser BJ, Veenhoven RH, Sanders EA, et al. The impact of breastfeeding on nasopharyngeal microbial communities in infants. Am J Respir Crit Care Med. 2014;190:298–308.PubMed 
    Article 

    Google Scholar 
    45.Bogaert D, Keijser B, Huse S, Rossen J, Veenhoven R, Van Gils E, et al. Variability and diversity of nasopharyngeal microbiota in children: a metagenomic analysis. PloS ONE. 2011;6:e17035.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    46.Bruce N, Perez-Padilla R, Albalak R. Indoor air pollution in developing countries: a major environmental and public health challenge. Bull World Health Organ. 2000;78:1078–92.PubMed 
    PubMed Central 
    CAS 

    Google Scholar 
    47.Pelissari DM, Diaz-Quijano FA. Household crowding as a potential mediator of socioeconomic determinants of tuberculosis incidence in Brazil. PloS ONE. 2017;12:e0176116.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    48.Mannucci PM, Franchini M. Health effects of ambient air pollution in developing countries. Int J Environ Res Public Health. 2017;14:1048.PubMed Central 
    Article 
    CAS 
    PubMed 

    Google Scholar 
    49.Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature.2012;486:222–7.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    50.Ferretti P, Pasolli E, Tett A, Asnicar F, Gorfer V, Fedi S, et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe. 2018;24:133–45.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    51.Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 2011;108:4680–7.PubMed 
    Article 

    Google Scholar 
    52.Mallick H, Rahnavard A, McIver LJ, Ma S, Zhang Y, Nguyen LH, et al. Multivariable association discovery in population-scale meta-omics studies. bioRxiv. 2021. https://doi.org/10.1101/2021.01.20.427420.53.Hojsak I, Snovak N, Abdović S, Szajewska H, Mišak Z, Kolaček S. Lactobacillus GG in the prevention of gastrointestinal and respiratory tract infections in children who attend day care centers: a randomized, double-blind, placebo-controlled trial. Clin Nutr. 2010;29:312–6.PubMed 
    Article 

    Google Scholar 
    54.Gluck U, Gebbers JO. Ingested probiotics reduce nasal colonization with pathogenic bacteria (Staphylococcus aureus, Streptococcus pneumoniae, and beta-hemolytic streptococci). Am J Clin Nutr. 2003;77:517–20.PubMed 
    Article 
    CAS 

    Google Scholar 
    55.Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy. 2007;37:498–505.PubMed 
    Article 
    CAS 

    Google Scholar 
    56.Nhan T-X, Parienti J-J, Badiou G, Leclercq R, Cattoir V. Microbiological investigation and clinical significance of Corynebacterium spp. in respiratory specimens. Diagn Microbiol Infect Dis. 2012;74:236–41.PubMed 
    Article 

    Google Scholar 
    57.Díez-Aguilar M, Ruiz-Garbajosa P, Fernández-Olmos A, Guisado P, Del Campo R, Quereda C, et al. Non-diphtheriae Corynebacterium species: an emerging respiratory pathogen. Eur J Clin Microbiol Infect Dis. 2013;32:769–72.PubMed 
    Article 
    CAS 

    Google Scholar 
    58.Teutsch B, Berger A, Marosevic D, Schönberger K, Lâm T-T, Hubert K, et al. Corynebacterium species nasopharyngeal carriage in asymptomatic individuals aged ≥ 65 years in Germany. Infection.2017;45:607–11.PubMed 
    Article 
    CAS 

    Google Scholar 
    59.Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinforma. 2009;10:421.Article 
    CAS 

    Google Scholar 
    60.Turner P, Turner C, Green N, Ashton L, Lwe E, Jankhot A, et al. Serum antibody responses to pneumococcal colonization in the first 2 years of life: results from an SE Asian longitudinal cohort study. Clin Microbiol Infect. 2013;19:e551–8.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    61.Numminen E, Chewapreecha C, Turner C, Goldblatt D, Nosten F, Bentley SD, et al. Climate induces seasonality in pneumococcal transmission. Sci Rep. 2015;5:11344.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    62.Kelly MS, Smieja M, Luinstra K, Wirth KE, Goldfarb DM, Steenhoff AP, et al. Association of respiratory viruses with outcomes of severe childhood pneumonia in Botswana. PloS ONE. 2015;10:e0126593.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    63.le Roux DM, Myer L, Nicol MP, Zar HJ. Incidence and severity of childhood pneumonia in the first year of life in a South African birth cohort: the Drakenstein Child Health Study. Lancet Glob Health. 2015;3:e95–103.PubMed 
    Article 

    Google Scholar 
    64.von Mollendorf C, von Gottberg A, Tempia S, Meiring S, de Gouveia L, Quan V, et al. Increased risk and mortality of invasive pneumococcal disease in HIV-exposed-uninfected infants More

  • in

    Transitional genomes and nutritional role reversals identified for dual symbionts of adelgids (Aphidoidea: Adelgidae)

    1.Szathmáry E, Smith JM. The major evolutionary transitions. Nature 1995;374:227–32.PubMed 
    Article 

    Google Scholar 
    2.West SA, Fisher RM, Gardner A, Kiers ET. Major evolutionary transitions in individuality. Proc Natl Acad Sci USA. 2015;112:10112–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    3.Moran NA. The coevolution of bacterial endosymbionts and phloem-feeding insects. Ann Mo Bot Gard. 2001;88:35–44.Article 

    Google Scholar 
    4.Bennett GM, Moran NA. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc Natl Acad Sci USA. 2015;112:10169–76.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    5.Gil R, Sabater-Munoz B, Latorre A, Silva FJ, Moya A. Extreme genome reduction in Buchnera spp.: toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci USA. 2002;99:4454–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Tamames J, Gil R, Latorre A, Pereto J, Silva FJ, Moya A. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol Biol. 2007;7:181.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    7.Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 2013;153:1567–78.CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Wilson ACC, Duncan RP. Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses. Proc Natl Acad Sci USA. 2015;112:10255–61.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    9.von Dohlen CD, Kohler S, Alsop ST, McManus WR. Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 2001;412:433–6.Article 

    Google Scholar 
    10.McCutcheon JP, McDonald BR, Moran NA. Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proc Natl Acad Sci USA. 2009;106:15394–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    11.Gatehouse LN, Sutherland P, Forgie SA, Kaji R, Christeller JT. Molecular and histological characterization of primary (Betaproteobacteria) and secondary (Gammaproteobacteria) endosymbionts of three mealybug species. Appl Environ Microbiol. 2012;78:1187–97.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    12.Bennett GM, Moran NA. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol Evol. 2013;5:1675–88.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    13.Bressan A, Mulligan KL. Localization and morphological variation of three bacteriome-inhabiting symbionts within a planthopper of the genus Oliarus (Hemiptera: Cixiidae): Bacteriome-inhabiting symbionts in Oliarus filicicola. Environ Microbiol Rep. 2013;5:499–505.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Bennett GM, Mao M. Comparative genomics of a quadripartite symbiosis in a planthopper host reveals the origins and rearranged nutritional responsibilities of anciently diverged bacterial lineages. Environ Microbiol. 2018;20:4461–72.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    15.von Dohlen CD, Spaulding U, Patch KB, Weglarz KM, Foottit RG, Havill NP, et al. Dynamic acquisition and loss of dual-obligate symbionts in the plant-sap-feeding Adelgidae (Hemiptera: Sternorrhyncha: Aphidoidea). Front Microbiol. 2017;8:1037.Article 

    Google Scholar 
    16.Mao M, Yang X, Poff K, Bennett G. Comparative genomics of the dual-obligate symbionts from the treehopper, Entylia carinata (Hemiptera: Membracidae), provide insight into the origins and evolution of an ancient symbiosis. Genome Biol Evol. 2017;9:1803–15.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    17.McCutcheon JP, Moran NA. Functional convergence in reduced genomes of bacterial symbionts spanning 200 my of evolution. Genome Biol Evol. 2010;2:708–18.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.McCutcheon JP, von Dohlen CD. An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Curr Biol. 2011;21:1366–72.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    19.Sloan DB, Moran NA. Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Mol Biol Evol. 2012;29:3781–92.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Hall AAG, Morrow JL, Fromont C, Steinbauer MJ, Taylor GS, Johnson SN, et al. Codivergence of the primary bacterial endosymbiont of psyllids versus host switches and replacement of their secondary bacterial endosymbionts. Environ Microbiol. 2016;18:2591–603.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    21.Tamas I, Klasson L, Canbäck B, Näslund AK, Eriksson A-S, Wernegreen JJ, et al. 50 million years of genomic stasis in endosymbiotic bacteria. Science 2002;296:2376–9.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 2000;407:81–6.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    23.Moran NA, Tran P, Gerardo NM. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Appl Environ Microbiol. 2005;71:8802–10.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    24.Gruwell ME, Hardy NB, Gullan PJ, Dittmar K. Evolutionary relationships among primary endosymbionts of the mealybug subfamily Phenacoccinae (Hemiptera: Coccoidea: Pseudococcidae). Appl Environ Microbiol. 2010;76:7521–5.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Koga R, Moran NA. Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont. ISME J. 2014;8:1237–46.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Mao M, Bennett GM. Symbiont replacements reset the co-evolutionary relationship between insects and their heritable bacteria. ISME J. 2020;14:1384–95.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Braendle C, Miura T, Bickel R, Shingleton AW, Kambhampati S, Stern DL. Developmental origin and evolution of bacteriocytes in the aphid–Buchnera symbiosis. PLoS Biol. 2003;1:e21.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Weglarz KM, Havill NP, Burke GR, von Dohlen CD. Partnering with a pest: genomes of hemlock woolly adelgid symbionts reveal atypical nutritional provisioning patterns in dual-obligate bacteria. Genome Biol Evol. 2018;10:1607–21.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Toenshoff ER, Penz T, Narzt T, Collingro A, Schmitz-Esser S, Pfeiffer S, et al. Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae). ISME J 2012;6:384–96.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.Toenshoff ER, Gruber D, Horn M. Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. Environ Microbiol. 2012;14:1284–95.CAS 
    PubMed 
    Article 

    Google Scholar 
    31.Toenshoff ER, Szabó G, Gruber D, Horn M. The pine bark adelgid, Pineus strobi, contains two novel bacteriocyte-associated gammaproteobacterial symbionts. Appl Environ Microbiol. 2014;80:878–85.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    32.von Dohlen CD, Spaulding U, Shields K, Havill NP, Rosa C, Hoover K. Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range. Environ Microbiol. 2013;15:2043–62.Article 
    CAS 

    Google Scholar 
    33.Havelka J, Danilov J, Rakauskas R. Relationships between aphid species of the family Adelgidae (Hemiptera Adelgoidea) and their endosymbiotic bacteria: a case study in Lithuania. Bull Insectology. 2021;74:1–10.
    Google Scholar 
    34.Favret C, Havill NP, Miller GL, Sano M, Victor B. Catalog of the adelgids of the world (Hemiptera, Adelgidae). Zookeys 2015;534:35–54.Article 

    Google Scholar 
    35.Blackman RL, Eastop VF Aphids on the world’s trees: an identification and information guide. 1994. CAB International.36.Havill NP, Foottit RG. Biology and evolution of Adelgidae. Ann Rev Ento. 2007;52:325–49.CAS 
    Article 

    Google Scholar 
    37.Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–20.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    38.Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: a fast and accurate Illumina paired-end read mergeR. Bioinformatics 2014;30:614–20.CAS 
    PubMed 
    Article 

    Google Scholar 
    39.Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comp Bio. 2012;19:455–77.CAS 
    Article 

    Google Scholar 
    40.Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE. 2014;9:e112963.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    41.Kolmogorov M, Yuan J, Lin Y, Pevzner PA. Assembly of long, error-prone reads using repeat graphs. Nat Biotechnol. 2019;37:540–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Laetsch DR, Blaxter ML. BlobTools: Interrogation of genome assemblies. F1000Research. 2017;6:1287.Article 

    Google Scholar 
    43.Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011;27:578–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    44.Chu C, Li X, Wu Y. GAPPadder: a sensitive approach for closing gaps on draft genomes with short sequence reads. BMC Genomics. 2019;20:426.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    45.Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014;30:2068–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    46.Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M. ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol. 2011;12:R30.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Karp PD, Billington R, Caspi R, Fulcher CA, Latendresse M, Kothari A, et al. The BioCyc collection of microbial genomes and metabolic pathways. Brief Bioinform. 2019;20:1085–93.CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Karp PD, Ong WK, Paley S, Billington R, Caspi R, Fulcher C, et al. The EcoCyc database. EcoSal Plus. 2018;8:10.1128.Article 

    Google Scholar 
    49.Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182–5.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ, von Mering C, et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol Biol Evol. 2017;34:2115–22.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28:33–36.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40:e49–e49.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Xu L, Dong Z, Fang L, Luo Y, Wei Z, Guo H, et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 2019;47:W52–W58.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Xu Y, Bi C, Wu G, Wei S, Dai X, Yin T, et al. VGSC: a web-based vector graph toolkit of genome synteny and collinearity. Biomed Res Int. 2016;2016:7823429.PubMed 
    PubMed Central 

    Google Scholar 
    55.Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol. 2016;66:5575–99.CAS 
    PubMed 
    Article 

    Google Scholar 
    56.Guy L. phyloSkeleton: taxon selection, data retrieval and marker identification for phylogenomics. Bioinformatics 2017;33:1230–2.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    57.Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol. 2011;7:e1002195.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009;25:1972–3.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    60.Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–3.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    61.Lartillot N, Rodrigue N, Stubbs D, Richer J. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol. 2013;62:611–5.CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Husník F, Chrudimský T, Hypša V. Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biology. 2011;9:1–17.Article 

    Google Scholar 
    63.Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.Hesse C, Schulz F, Bull CT, Shaffer BT, Yan Q, Shapiro N, et al. Genome-based evolutionary history of Pseudomonas spp. Environ Microbiol. 2018;20:2142–59.CAS 
    PubMed 
    Article 

    Google Scholar 
    65.Burke GR, Normark BB, Favret C, Moran NA. Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. Appl Environ Microbiol. 2009;75:5328–35.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Manzano‐Marín A, Szabó G, Simon J, Horn M, Latorre A. Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids: co-obligate endosymbiont dynamics in the Lachninae. Environ Microbiol. 2017;19:393–408.PubMed 
    Article 
    CAS 

    Google Scholar 
    67.Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52.CAS 
    PubMed 
    Article 

    Google Scholar 
    68.ggplot2. Create elegant data visualisations using the grammar of graphics. https://ggplot2.tidyverse.org/. Accessed Apr 2021.69.Manzano-Marín A, Oceguera-Figueroa A, Latorre A, Jiménez-García LF, Moya A. Solving a bloody mess: B-vitamin independent metabolic convergence among gammaproteobacterial obligate endosymbionts from blood-feeding arthropods and the leech Haementeria officinalis. Genome Biol Evol. 2015;7:2871–84.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    70.Janda JM, Abbott SL. The genus Hafnia: from soup to nuts. Clin Microbiol Rev. 2006;19:12–18.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Szabó G, Schulz F, Manzano-Marín A, Toenshoff ER, Horn M Evolutionary recent dual obligatory symbiosis among adelgids indicates a transition between fungus and insect associated lifestyles. bioRxiv. 2020; e-pub ahead of print 16 October 2020; https://doi.org/10.1101/2020.10.16.342642.72.Wilson ACC, Ashton PD, Calevro F, Charles H, Colella S, Febvay G, et al. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol. 2010;19:249–58.CAS 
    PubMed 
    Article 

    Google Scholar 
    73.Sloan DB, Nakabachi A, Richards S, Qu J, Murali SC, Gibbs RA, et al. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol Biol Evol. 2014;31:857–71.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Hansen AK, Moran NA. The impact of microbial symbionts on host plant utilization by herbivorous insects. Mol Ecol. 2014;23:1473–96.PubMed 
    Article 

    Google Scholar 
    75.Manzano-Marı́n A, Coeur d’acier A, Clamens A-L, Orvain C, Cruaud C, Barbe V, et al. Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems. ISME J. 2020;14:259–73.Article 
    CAS 

    Google Scholar 
    76.Lo W-S, Huang Y-Y, Kuo C-H. Winding paths to simplicity: genome evolution in facultative insect symbionts. FEMS Microbiol Rev. 2016;40:855–74.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Toh H, Weiss BL, Perkin SAH, Yamashita A, Oshima K, Hattori M, et al. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res. 2006;16:149–56.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, et al. Massive gene decay in the leprosy bacillus. Nature 2001;409:1007–11.CAS 
    PubMed 
    Article 

    Google Scholar 
    79.Moran NA, Bennett GM. The tiniest tiny genomes. Annu Rev Microbiol. 2014;68:195–215.CAS 
    PubMed 
    Article 

    Google Scholar 
    80.Bennett GM, McCutcheon JP, MacDonald BR, Romanovicz D, Moran NA. Differential genome evolution between companion symbionts in an insect-bacterial symbiosis. mBio 2014;5:e01697–14.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.Degnan PH, Ochman H, Moran NA. Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont Buchnera. PLoS Genet. 2011;7:e1002252.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Van Leuven JT, Meister RC, Simon C, McCutcheon JP. Sympatric speciation in a bacterial endosymbiont results in two genomes with the functionality of one. Cell 2014;158:1270–80.PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    83.Gomez-Valero L. The evolutionary fate of nonfunctional DNA in the bacterial endosymbiont Buchnera aphidicola. Mol Biol Evol. 2004;21:2172–81.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    84.Manzano-Marı́n A, Coeur d’acier A, Clamens A-L, Orvain C, Cruaud C, Barbe V, et al. A freeloader? The highly eroded yet large genome of the Serratia symbiotica symbiont of Cinara strobi. Genome Biol Evol. 2018;10:2178–89.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    85.Santos-Garcia D, Silva FJ, Morin S, Dettner K, Kuechler SM. The all-rounder Sodalis: a new bacteriome-associated endosymbiont of the lygaeoid bug Henestaris halophilus (Heteroptera: Henestarinae) and a critical examination of its evolution. Genome Biol Evol. 2017;9:2893–910.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Havill NP, Foottit RG, von Dohlen CD. Evolution of host specialization in the Adelgidae (Insecta: Hemiptera) inferred from molecular phylogenetics. Mol Phylogenet. 2007;44:357–70.CAS 
    Article 

    Google Scholar 
    87.Manzano-Marı́n A, Latorre A. Snapshots of a shrinking partner: genome reduction in Serratia symbiotica. Sci Rep. 2016;6:32590.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    88.Monnin D, Jackson R, Kiers ET, Bunker M, Ellers J, Henry LM. Parallel evolution in the integration of a co-obligate aphid symbiosis. Curr Biol. 2020;30:1949–57. e6CAS 
    PubMed 
    Article 

    Google Scholar 
    89.Husnik F, McCutcheon JP. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proc Natl Acad Sci USA. 2016;113:e5416–24.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    90.Moran NA, McCutcheon JP, Nakabachi A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet. 2008;42:165–90.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    91.Degnan PH, Leonardo TE, Cass BN, Hurwitz B, Stern D, Gibbs RA, et al. Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol. 2010;12:2060–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    92.Burke GR, Moran NA. Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol. 2011;3:195–208.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    93.Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, et al. Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol. 1991;173:6321–4.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    94.Moran NA, Munson MA, Baumann P, Ishikawa H. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proc R Soc B 1993;253:167–71.Article 

    Google Scholar 
    95.Kuechler SM, Gibbs G, Burckhardt D, Dettner K, Hartung V. Diversity of bacterial endosymbionts and bacteria-host co-evolution in Gondwanan relict moss bugs (Hemiptera: Coleorrhyncha: Peloridiidae). Environ Microbiol. 2013;15:2031–42.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    96.Thao ML, Moran NA, Abbot P, Brennan EB, Burckhardt DH, Baumann P. Cospeciation of psyllids and their primary prokaryotic endosymbionts. Appl Environ Microbiol. 2000;66:2898–905.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Thao ML, Baumann P. Evolutionary relationships of primary prokaryotic endosymbionts of whiteflies and their hosts. Appl Environ Microbiol. 2004;70:3401–6.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    98.Meseguer AS, Manzano-Marín A, Coeur d’Acier A, Clamens AL, Godefroid M, Jousselin E. Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts. Mol Ecol. 2017;26:2363–78.CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    99.McCutcheon JP, Moran NA. Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA. 2007;104:19392–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    100.Rao Q, Rollat-Farnier PA, Zhu DT, Santos-Garcia D, Silva FJ, Moya A, et al. Genome reduction and potential metabolic complementation of the dual endosymbionts in the whitefly Bemisia tabaci. BMC Genomics. 2015;16:226.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    101.Rosenblueth M, Sayavedra L, Sámano-Sánchez H, Roth A, Martínez-Romero E. Evolutionary relationships of flavobacterial and enterobacterial endosymbionts with their scale insect hosts (Hemiptera: Coccoidea). J Evol Biol. 2012;25:2357–68.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    102.Michalik K, Szklarzewicz T, Kalandyk-Kołodziejczyk M, Jankowska W, Michalik A. Bacteria belonging to the genus Burkholderia are obligatory symbionts of the eriococcids Acanthococcus aceris Signoret, 1875 and Gossyparia spuria (Modeer, 1778) (Insecta, Hemiptera, Coccoidea). Arthropod Struct Dev. 2016;45:265–72.PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    103.Van Ham RC, Kamerbeek J, Palacios C, Rausell C, Abascal F, Bastolla U, et al. Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci USA. 2003;100:581–6.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    104.Vogel KJ, Moran NA. Effect of host genotype on symbiont titer in the aphid-Buchnera symbiosis. Insects 2011;2:423–34.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    105.Bennett GM, McCutcheon JP, McDonald BR, Moran NA. Lineage-specific patterns of genome deterioration in obligate symbionts of sharpshooter leafhoppers. Genome Biol Evol. 2015;8:296–301.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    106.Havill NP, Griffin BP, Andersen JC, Foottit RG, Justesen MJ, Caccone A, et al. Species delimitation and invasion history of the balsam woolly adelgid, Adelges (Dreyfusia) piceae (Hemiptera: Aphidoidea: Adelgidae), species complex. Syst Entomol. 2021;46:186–204.Article 

    Google Scholar  More

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    Selective feeding in Southern Ocean key grazers—diet composition of krill and salps

    1.Pakhomov, E. A., Froneman, P. W. & Perissinotto, R. Salp/krill interactions in the Southern Ocean: Spatial segregation and implications for the carbon flux. Deep Sea Res. II 49, 1881–1907 (2002).CAS 
    Article 

    Google Scholar 
    2.Steinberg, D. K. et al. Long-term (1993–2013) changes in macrozooplankton off the Western Antarctic Peninsula. Deep Sea Res. I 101, 54–70 (2015).Article 

    Google Scholar 
    3.Whitehouse, M. J. et al. Role of krill versus bottom-up factors in controlling phytoplankton biomass in the northern Antarctic waters of South Georgia. Mar. Ecol. Prog. Ser. 393, 69–82 (2009).CAS 
    Article 

    Google Scholar 
    4.Tarling, G. A. & Fielding, S. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 279–319 (Springer International Publishing, 2016).5.Henschke, N., Everett, J. D., Richardson, A. J. & Suthers, I. M. Rethinking the role of salps in the ocean. Trends Ecol. Evol. 31, 720–733 (2016).PubMed 
    Article 

    Google Scholar 
    6.Cavan, E. L. et al. The importance of Antarctic krill in biogeochemical cycles. Nat. Commun. 10, 4742 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Belcher, A. et al. Krill faecal pellets drive hidden pulses of particulate organic carbon in the marginal ice zone. Nat. Commun. 10, 889 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Phillips, B., Kremer, P. & Madin, L. P. Defecation by Salpa thompsoni and its contribution to vertical flux in the Southern Ocean. Mar. Biol. 156, 455–467 (2009).Article 

    Google Scholar 
    9.Siegel, V. & Watkins, J. L. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 21–100 (Springer International Publishing, 2016).10.Atkinson, A. et al. Krill (Euphausia superba) distribution contracts southward during rapid regional warming. Nat. Clim. Change 9, 142–147 (2019).Article 

    Google Scholar 
    11.Vaughan, D. G. et al. Recent rapid regional climate warming on the Antarctic Peninsula. Clim. Change 60, 243–274 (2003).Article 

    Google Scholar 
    12.Ducklow, H. W. et al. Marine pelagic ecosystems: the West Antarctic Peninsula. Philos. Trans. R. Soc. B. 362, 67–94 (2007).Article 

    Google Scholar 
    13.Montes-Hugo, M. et al. Recent changes in phytoplankton communities associated with rapid regional climate change along the Western Antarctic Peninsula. Science 323, 1470–1473 (2009).CAS 
    PubMed 
    Article 

    Google Scholar 
    14.Clarke, A. et al. Climate change and the marine ecosystem of the western Antarctic Peninsula. Philos. T. R. Soc., B 362, 149–166 (2007).Article 

    Google Scholar 
    15.Atkinson, A., Siegel, V., Pakhomov, E. & Rothery, P. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432, 100–103 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    16.Loeb, V. et al. Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387, 897–900 (1997).CAS 
    Article 

    Google Scholar 
    17.Flores, H. et al. Impact of climate change on Antarctic krill. Mar. Ecol. Prog. Ser. 458, 1–19 (2012).Article 

    Google Scholar 
    18.Cox, M. J. et al. No evidence for a decline in the density of Antarctic krill Euphausia superba Dana, 1850, in the Southwest Atlantic sector between 1976 and 2016. J. Crust. Biol. 38, 656–661 (2018).19.Foxton, P. The Distribution and Life-history of Salpa thompsoni Foxton with observations on a Related Species, Salpa gerlachei Foxton (The University Press, 1966).20.Bernard, K. S., Steinberg, D. K. & Schofield, O. M. E. Summertime grazing impact of the dominant macrozooplankton off the Western Antarctic Peninsula. Deep Sea Res. I 62, 111–122 (2012).Article 

    Google Scholar 
    21.Condon, R. H. et al. Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc. Natl Acad. Sci. 108, 10225–10230 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    22.Meyer, M. A. & Elsayed, S. Z. Grazing of Euphausia superba Dana on natural phytoplankton populations. Polar Biol. 1, 193–197 (1983).Article 

    Google Scholar 
    23.Haberman, K. L., Ross, R. M. & Quetin, L. B. Diet of the Antarctic krill (Euphausia superba Dana): II. Selective grazing in mixed phytoplankton assemblages. J. Exp. Mar. Biol. Ecol. 283, 97–113 (2003).Article 

    Google Scholar 
    24.Schmidt, K. & Atkinson, A. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 175–224 (Springer International Publishing, 2016).25.Andersen, V. in The Biology of Pelagic Tunicates (ed Bone, Q.) 125–137 (Oxford University Press, 1998).26.Mitra, A. et al. Bridging the gap between marine biogeochemical and fisheries sciences; configuring the zooplankton link. Prog. Oceanogr. 129, 176–199 (2014).Article 

    Google Scholar 
    27.Sailley, S. F., Polimene, L., Mitra, A., Atkinson, A. & Allen, J. I. Impact of zooplankton food selectivity on plankton dynamics and nutrient cycling. J. Plankton Res. 37, 519–529 (2015).CAS 
    Article 

    Google Scholar 
    28.Hamner, W. M., Hamner, P. P., Strand, S. W. & Gilmer, R. W. Behavior of Antarctic krill, Euphausia superba: Chemoreception, feeding, schooling, and molting. Science 220, 433–435 (1983).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.DeMott, W. R. in Behavioural Mechanisms of Food Selection (ed Hughes, R. N.) 569–594 (Springer, 1990).30.Le Fèvre, J., Legendre, L. & Rivkin, R. B. Fluxes of biogenic carbon in the Southern Ocean: Roles of large microphagous zooplankton. J. Mar. Syst. 17, 325–345 (1998).Article 

    Google Scholar 
    31.Moline, M. A., Claustre, H., Frazer, T. K., Schofield, O. & Vernet, M. Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Glob. Change Biol. 10, 1973–1980 (2004).Article 

    Google Scholar 
    32.Frischer, M. E. et al. Selective feeding and linkages to the microbial food web by the doliolid Dolioletta gegenbauri. Limnol. Oceanogr. 66, 1993–2010 (2021).Article 

    Google Scholar 
    33.Dadon-Pilosof, A., Lombard, F., Genin, A., Sutherland, K. R. & Yahel, G. Prey taxonomy rather than size determines salp diets. Limnol. Oceanogr. 64, 1996–2010 (2019).Article 

    Google Scholar 
    34.Metfies, K., Nicolaus, A., von Harbou, L., Bathmann, U. & Peeken, I. Molecular analyses of gut contents: elucidating the feeding of co-occurring salps in the Lazarev Sea from a different perspective. Antarct. Sci. 26, 5545–5553 (2014).Article 

    Google Scholar 
    35.Cleary, A. C., Durbin, E. G. & Casas, M. C. Feeding by Antarctic krill Euphausia superba in the West Antarctic Peninsula: differences between fjords and open waters. Mar. Ecol. Prog. Ser. 595, 39–54 (2018).CAS 
    Article 

    Google Scholar 
    36.Pompanon, F. et al. Who is eating what: Diet assessment using next generation sequencing. Mol. Ecol. 21, 1931–1950 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    37.Passmore, A. J. et al. DNA as a dietary biomarker in Antarctic krill, Euphausia superba. Mar. Biotechnol. 8, 686–696 (2006).CAS 
    Article 

    Google Scholar 
    38.von Harbou, L. et al. Salps in the Lazarev Sea, Southern Ocean: I. Feeding dynamics. Mar. Biol. 158, 2009–2026 (2011).Article 

    Google Scholar 
    39.Vernet, M. et al. Primary production throughout austral fall, during a time of decreasing daylength in the western Antarctic Peninsula. Mar. Ecol. Prog. Ser. 452, 45–61 (2012).CAS 
    Article 

    Google Scholar 
    40.Moreau, S. et al. Variability of the microbial community in the western Antarctic Peninsula from late fall to spring during a low ice cover year. Polar Biol. 33, 1599–1614 (2010).Article 

    Google Scholar 
    41.Selz, V. et al. Distribution of Phaeocystis antarctica-dominated sea ice algal communities and their potential to seed phytoplankton across the western Antarctic Peninsula in spring. Mar. Ecol. Prog. Ser. 586, 91–112 (2018).CAS 
    Article 

    Google Scholar 
    42.Nichols, D. S., Nichols, P. D. & Sullivan, C. W. Fatty acid, sterol and hydrocarbon composition of Antarctic sea ice diatom communities during the spring bloom in McMurdo Sound. Antarct. Sci. 5, 271–278 (1993).Article 

    Google Scholar 
    43.Fahl, K. & Kattner, G. Lipid Content and fatty acid composition of algal communities in sea-ice and water from the Weddell Sea (Antarctica). Polar Biol. 13, 405–409 (1993).Article 

    Google Scholar 
    44.Boyd, C. M., Heyraud, M. & Boyd, C. N. Feeding of the Antarctic krill Euphausia superba. J. Crust. Biol. 4, 123–141 (1984).Article 

    Google Scholar 
    45.Bone, Q., Carré, C. & Chang, P. Tunicate feeding filters. J. Mar. Biol. Assoc. U. K. 83, 907–919 (2003).Article 

    Google Scholar 
    46.Nelson, M. M., Phleger, C. F., Mooney, B. D. & Nichols, P. D. Lipids of gelatinous Antarctic zooplankton: Cnidaria and Ctenophora. Lipids 35, 551–559 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    47.Huntley, M. E., Sykes, P. F. & Marin, V. Biometry and trophodynamics of Salpa thompsoni Foxton (Tunicata: Thaliacea) near the Antarctic Peninsula in austral summer, 1983–1984. Polar Biol. 10, 59–70 (1989).Article 

    Google Scholar 
    48.Hopkins, T. L. Food web of an Antarctic midwater ecosystem. Mar. Biol. 89, 197–212 (1985).Article 

    Google Scholar 
    49.Paffenhöfer, G. A. & Köster, M. Digestion of diatoms by planktonic copepods and doliolids. Mar. Ecol. Prog. Ser. 297, 303–310 (2005).Article 

    Google Scholar 
    50.von Harbou, L. Trophodynamics of Salps in the Atlantic Southern Ocean. PhD thesis, University of Bremen (2009).51.Hargraves, P. E. The ebridian flagellates Ebria and Hermesinum. Plankton Biol. Ecol. 49, 9–16 (2002).
    Google Scholar 
    52.Cavan, E. L. et al. Attenuation of particulate organic carbon flux in the Scotia Sea, Southern Ocean, is controlled by zooplankton fecal pellets. Geophys. Res. Lett. 42, 821–830 (2015).CAS 
    Article 

    Google Scholar 
    53.Smith, K. L. Jr. et al. Large salp bloom export from the upper ocean and benthic community response in the abyssal northeast Pacific: day to week resolution. Limnol. Oceanogr. 59, 745–757 (2014).CAS 
    Article 

    Google Scholar 
    54.Cadée, G. C., González, H. & Schnack-Schiel, S. B. Krill diet affects faecal string settling. Polar Biol. 12, 75–80 (1992).
    Google Scholar 
    55.Ploug, H., Iversen, M. H., Koski, M. & Buitenhuis, E. T. Production, oxygen respiration rates, and sinking velocity of copepod fecal pellets: Direct measurements of ballasting by opal and calcite. Limnol. Oceanogr. 53, 469–476 (2008).CAS 
    Article 

    Google Scholar 
    56.Atkinson, A., Schmidt, K., Fielding, S., Kawaguchi, S. & Geissler, P. A. Variable food absorption by Antarctic krill: Relationships between diet, egestion rate and the composition and sinking rates of their fecal pellets. Deep Sea Res. II 59-60, 147–158 (2012).CAS 
    Article 

    Google Scholar 
    57.Schmidt, K., Atkinson, A., Pond, D. W. & Ireland, L. C. Feeding and overwintering of Antarctic krill across its major habitats: The role of sea ice cover, water depth, and phytoplankton abundance. Limnol. Oceanogr. 59, 17–36 (2014).Article 

    Google Scholar 
    58.Cripps, G. C., Watkins, J. L., Hill, H. J. & Atkinson, A. Fatty acid content of Antarctic krill Euphausia superba at South Georgia related to regional populations and variations in diet. Mar. Ecol. Prog. Ser. 181, 177–188 (1999).CAS 
    Article 

    Google Scholar 
    59.Schmidt, K., Atkinson, A., Petzke, K.-J., Voss, M. & Pond, D. W. Protozoans as a food source for Antarctic krill, Euphausia superba: Complementary insights from stomach content, fatty acids, and stable isotopes. Limnol. Oceanogr. 51, 2409–2427 (2006).CAS 
    Article 

    Google Scholar 
    60.Hagen, W., Van Vleet, E. S. & Kattner, G. Seasonal lipid storage as overwintering strategy of Antarctic krill. Mar. Ecol. Prog. Ser. 134, 85–89 (1996).CAS 
    Article 

    Google Scholar 
    61.Kawaguchi, S. & Takahashi, Y. Antarctic krill (Euphausia superba Dana) eat salps. Polar Biol. 16, 479–481 (1996).
    Google Scholar 
    62.Clarke, L. J., Bestley, S., Bissett, A. & Deagle, B. E. A globally distributed Syndiniales parasite dominates the Southern Ocean micro-eukaryote community near the sea-ice edge. ISME J. 13, 734–737 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Coats, D. W. & Park, M. G. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): Parasite survival, infectivity, generation time, and host specificity. J. Phycol. 38, 520–528 (2002).Article 

    Google Scholar 
    64.Sutherland, K. R., Madin, L. P. & Stocker, R. Filtration of submicrometer particles by pelagic tunicates. Proc. Natl Acad. Sci. 107, 15129–15134 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.Gómez-Gutiérrez, J. & Morales-Avila, J. R. in Biology and Ecology of Antarctic krill (ed Siegel, V.) 351–387 (Springer International Publishing, 2006).66.Cleary, A. C., Casas, M. C., Durbin, E. G. & Gómez-Gutiérrez, J. Parasites in Antarctic krill guts inferred from DNA sequences. Antarct. Sci. 31, 16–22 (2019).Article 

    Google Scholar 
    67.Zamora-Terol, S., Novotny, A. & Winder, M. Molecular evidence of host-parasite interactions between zooplankton and Syndiniales. Aquat. Ecol. 55, 125–134 (2021).CAS 
    Article 

    Google Scholar 
    68.Kawaguchi, S., Ichii, T. & Naganobu, M. Do krill and salps compete? Contrary evidence from the krill fisheries. CCAMLR Sci. 5, 205–216 (1998).
    Google Scholar 
    69.Fadeev, E. et al. Microbial communities in the east and west Fram Strait during sea ice melting season. Front. Mar. Sci. 5, 429 (2018).Article 

    Google Scholar 
    70.Vestheim, H. & Jarman, S. N. Blocking primers to enhance PCR amplification of rare sequences in mixed samples – a case study on prey DNA in Antarctic krill stomachs. Front. Zool. 5, 12 (2008).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    71.Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363–1371 (2004).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    72.R Foundation for Statistical Computing. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).73.Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Callahan, B. DADA2 Pipeline Tutorial (1.16), available online: https://benjjneb.github.io/dada2/tutorial.html. Accessed: 3 Feb 2020.75.Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 3 (2011).Article 

    Google Scholar 
    76.Guillou, L. et al. The protist ribosomal reference database (PR2): A catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 41, D597–D604 (2013).CAS 
    PubMed 
    Article 

    Google Scholar 
    77.Gong, W. & Marchetti, A. Estimation of 18S gene copy number in marine eukaryotic plankton using a next-generation sequencing approach. Front. Mar. Sci. 6, 219 (2019).Article 

    Google Scholar 
    78.Metfies, K. et al. Uncovering the intricacies of microbial community dynamics at Helgoland Roads at the end of a spring bloom using automated sampling and 18S meta-barcoding. PLoS ONE 15, e0233921 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    79.Catlett, D. et al. Evaluation of accuracy and precision in an amplicon sequencing workflow for marine protist communities. Limnol. Oceanogr. Methods 18, 20–40 (2019).Article 

    Google Scholar 
    80.Kattner, G. & Fricke, H. S. G. Simple gas-liquid-chromatographic method for the simultaneous determination of fatty-acids and alcohols in wax esters of marine organisms. J. Chromatogr. 361, 263–268 (1986).CAS 
    Article 

    Google Scholar 
    81.Gloor, G. B., Macklaim, J. M., Pawlowsky-Glahn, V. & Egozcue, J. J. Microbiome datasets are compositional: And this is not optional. Front. Microbiol. 8, 2224 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Palarea-Albaladejo, J. & Martín-Fernández, J. A. zCompositions—R package for multivariate imputation of left-censored data under a compositional approach. Chemometrics Intell. Lab. Syst. 143, 85–96 (2015).CAS 
    Article 

    Google Scholar 
    83.Fernandes, A. D., Macklaim, J. M., Linn, T. G., Reid, G. & Gloor, G. B. ANOVA-Like differential expression (ALDEx) analysis for mixed population RNA-Seq. PLoS ONE 8, e67019 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    84.Quinn, T. P., Richardson, M. F., Lovell, D. & Crowley, T. M. propr: an R-package for identifying proportionally abundant features using compositional data analysis. Sci. Rep. 7, 16252 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    85.Bian, G. et al. The gut microbiota of healthy aged chinese is similar to that of the healthy young. mSphere 2, e00327–00317 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Gloor, G. B. & Reid, G. Compositional analysis: A valid approach to analyze microbiome high-throughput sequencing data. Can. J. Microbiol. 62, 692–703 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    87.Borstein, S. R. dietr: An R package for calculating fractional trophic levels from quantitative and qualitative diet data. Hydrobiologia 847, 4285–4294 (2020).Article 

    Google Scholar 
    88.Lechowicz, M. J. The sampling characteristics of electivity indices. Oecologia 52, 22–30 (1982).PubMed 
    Article 

    Google Scholar 
    89.Dalsgaard, J., St John, M., Kattner, G., Muller-Navarra, D. & Hagen, W. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46, 225–340 (2003).PubMed 
    Article 

    Google Scholar 
    90.Graeve, M., Kattner, G. & Hagen, W. Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: Experimental evidence of trophic markers. J. Exp. Mar. Biol. Ecol. 182, 97–110 (1994).CAS 
    Article 

    Google Scholar 
    91.Kharlamenko, V. I., Zhukova, N. V., Khotimchenko, S. V., Svetashev, V. I. & Kamenev, G. M. Fatty acids as markers of food sources in a shallow-water hydrothermal ecosystem (Kraternaya Bight, Yankich Island, Kurile Islands). Mar. Ecol. Prog. Ser. 120, 231–241 (1995).CAS 
    Article 

    Google Scholar 
    92.Greenacre, M. Compositional Data Analysis in Practice (CRC Press, Taylor & Francis Group, 2018).93.Suh, H.-L. & Nemoto, T. Comparative morphology of filtering structure of five species of Euphausia (Euphausiacea, Crustacea) from the Antarctic Ocean. Proc. NIPR Symp. Polar Biol. 1, 72–83 (1987).
    Google Scholar 
    94.Alldredge, A. L. & Madin, L. P. Pelagic tunicates: unique herbivores in the marine plankton. Bioscience 32, 655–663 (1982).Article 

    Google Scholar 
    95.Kelly, P. S. The Ecological Role of Salpa Thompsoni in the Kerguelen Plateau Region of the Southern Ocean: A First Comprehensive Evaluation. PhD thesis, University of Tasmania (2019).96.Ericson, J. A. et al. Seasonal and interannual variations in the fatty acid composition of adult Euphausia superba Dana, 1850 (Euphausiacea) samples derived from the Scotia Sea krill fishery. J. Crust. Biol. 38, 662–672 (2018).
    Google Scholar 
    97.Martin, D. L., Ross, R. M., Quetin, L. B. & Murray, A. E. Molecular approach (PCR-DGGE) to diet analysis in young Antarctic krill Euphausia superba. Mar. Ecol. Prog. Ser. 319, 155–165 (2006).CAS 
    Article 

    Google Scholar 
    98.Matsuoka, K. et al. Quantarctica, an integrated mapping environment for Antarctica, the Southern Ocean, and sub-Antarctic islands. Environ. Model. Softw. 140, 105015 (2021).Article 

    Google Scholar  More

  • in

    Historical land use has long-term effects on microbial community assembly processes in forest soils

    1.Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol. 2017;15:579–90.CAS 
    Article 

    Google Scholar 
    2.Ellis EC. Anthropogenic transformation of the terrestrial biosphere. Philos Trans R Soc A-Math Phys Eng Sci. 2011;369:1010–35.Article 

    Google Scholar 
    3.Jangid K, Williams MA, Franzluebbers AJ, Schmidt TM, Coleman DC, Whitman WB. Land-use history has a stronger impact on soil microbial community composition than aboveground vegetation and soil properties. Soil Biol Biochem. 2011;43:2184–93.CAS 
    Article 

    Google Scholar 
    4.Ramirez KS, Lauber CL, Knight R, Bradford MA, Fierer N. Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology. 2010;91:3463–70.Article 

    Google Scholar 
    5.Hermans SM, Taylor M, Grelet G, Curran-Cournane F, Buckley HL, Handley KM, et al. From pine to pasture: land use history has long-term impacts on soil bacterial community composition and functional potential. FEMS Microbiol Ecol. 2020;96:1–12.6.Keiser AD, Knoepp JD, Bradford MA. Disturbance decouples biogeochemical cycles across forests of the Southeastern US. Ecosystems. 2016;19:50–61.Article 

    Google Scholar 
    7.Goss-Souza D, Mendes LW, Borges CD, Baretta D, Tsai SM, Rodrigues J. Soil microbial community dynamics and assembly under long-term land use change. FEMS Microbiol Ecol. 2017;93:1–13.8.Tripathi BM, Stegen JC, Kim M, Dong K, Adams JM, Lee YK. Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. The ISME Journal. 2018;12:1072–83.CAS 
    Article 

    Google Scholar 
    9.Barnett SE, Youngblut ND, Buckley DH. Soil characteristics and land-use drive bacterial community assembly patterns. FEMS Microbiol Ecol. 2020;96:1–11.10.Osburn ED, McBride SG, Aylward FO, Badgley BD, Strahm BD, Knoepp JD, et al. Soil bacterial and fungal communities exhibit distinct long-term responses to disturbance in temperate forests. Front Microbiol. 2019;10:2872.11.Pruesse E, Peplies J, Glöckner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics. 2012;28:1823–9.CAS 
    Article 

    Google Scholar 
    12.Mirarab S, Nguyen N, Guo S, Wang LS, Kim J, Warnow T, et al. PASTA: ultra-large multiple sequence alignment for nucleotide and amino-acid sequences. J Comput Biol. 2014;22:377–86.Article 

    Google Scholar 
    13.Wang P, Li SP, Yang X, Zhou J, Shu W, Jiang L. Mechanisms of soil bacterial and fungal community assembly differ among and within islands. Environ Microbiol. 2020;22:1559–71.Article 

    Google Scholar 
    14.Price MN, Dehal PS, Arkin AP. FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490.Article 

    Google Scholar 
    15.Stegen JC, Lin X, Fredrickson JK, Chen X, Kennedy DW, Murray CJ, et al. Quantifying community assembly processes and identifying features that impose them. ISME J. 2013;7:2069–79.Article 

    Google Scholar 
    16.Fillinger L, Hug K, Griebler, C. Selection imposed by local environmental conditions drives differences in microbial community composition across geographically distinct groundwater aquifers. FEMS Microbiol. Ecol. 2019;95:1–12.17.Powell JR, Karunaratne S, Campbell CD, Yao H, Robinson L, Singh BK. Deterministic processes vary during community assembly for ecologically dissimilar taxa. Nat Commun. 2015;6:8444.CAS 
    Article 

    Google Scholar 
    18.Peay KG, Schubert MG, Nguyen NH, Bruns TD. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol. 2012;21:4122–36.Article 

    Google Scholar 
    19.Elliott KJ, Vose JM. The contribution of the Coweeta Hydrologic Laboratory to developing an understanding of long-term (1934-2008) changes in managed and unmanaged forests. For Ecol Manag. 2011;261:900–10.Article 

    Google Scholar 
    20.Zhang X, Johnston ER, Liu W, Li L, Han X. Environmental changes affect the assembly of soil bacterial community primarily by mediating stochastic processes. Global Change Biology. 2016;22:198–207.Article 

    Google Scholar 
    21.Dini-Andreote F, Stegen JC, Elsas JD, van, Salles JF. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc Natl Acad Sci USA. 2015;112:E1326–32.CAS 
    Article 

    Google Scholar  More

  • in

    Twenty-year trends in antimicrobial resistance from aquaculture and fisheries in Asia

    We reviewed and mapped antimicrobial resistance in aquatic food animals in Asia during a period of substantial industry growth. Our findings indicate that between 2000 and 2018, antimicrobial resistance in bacteria from cultured aquatic food animals was stable (33%) while the resistance from wild-caught aquatic food animals decreased sharply (52% to 22%). These trends represent currently available evidence from point prevalence surveys, which serve as a surrogate in the absence of systematic surveillance and should be interpreted cautiously. Structured, systematic surveillance will be imperative to document trends in multi-drug resistance at the sub-national level in the future.Our results are consistent with an analysis of antimicrobial resistance in aquaculture-derived bacteria from forty countries, nearly half of which in Asia, which identified a global mean multi-antibiotic resistance index of .25, and a higher index ( >.35) in low-income and middle-income countries in Asia27. Although antimicrobial use in surveys from cultured animals was most frequently unspecified, in the limited surveys that recorded whether on-farm antimicrobials were either used or not used (n = 63; 11%), use was associated with higher multi-drug resistance than the absence of use (p  More

  • in

    Future phytoplankton diversity in a changing climate

    1.Food and Agriculture Organization of the United Nations. The State of World Fisheries and Aquaculture http://www.fao.org/3/i2727e/i2727e00.htm (2012).2.Isbell, F. et al. Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526, 574–577 (2015).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    3.IPBES. Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services https://doi.org/10.5281/zenodo.3553579 (2019).4.Tittensor, D. P. et al. A mid-term analysis of progress toward international biodiversity targets. Science 346, 241–244 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Dornelas, M. et al. Assemblage time series reveal biodiversity change but not systematic loss. Science 344, 296–299 (2014).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    6.Gonzalez, A. et al. Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity. Ecology 97, 1949–1960 (2016).PubMed 
    Article 

    Google Scholar 
    7.Elahi, R. et al. Recent trends in local-scale marine biodiversity reflect community structure and human impacts. Curr. Biol. 25, 1938–1943 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Blowes, S. A. et al. The geography of biodiversity change in marine and terrestrial assemblages. Science 366, 339–345 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    9.McCann, K. S. The diversity–stability debate. Nature 405, 228–233 (2000).CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Loreau, M. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804–808 (2001).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    11.Covich, A. P. et al. The role of biodiversity in the functioning of freshwater and marine benthic ecosystems. Bioscience 54, 767–775 (2004).Article 

    Google Scholar 
    12.Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35 (2005).Article 

    Google Scholar 
    13.Widdicombe, C. E., Eloire, D., Harbour, D., Harris, R. P. & Somerfield, P. J. Long-term phytoplankton community dynamics in the Western English Channel. J. Plankton Res. 32, 643–655 (2010).Article 

    Google Scholar 
    14.Eloire, D. et al. Temporal variability and community composition of zooplankton at station L4 in the Western Channel: 20 years of sampling. J. Plankton Res. 32, 657–679 (2010).Article 

    Google Scholar 
    15.Hillebrand, H. et al. In Handbook on Marine Environment Protection (eds Salomon, M. & Markus, T.) 21 (Springer, 2018).16.Bindoff, N. L. et al. In IPCC Special Report on the Ocean and Cryosphere in a Changing Climate (eds H.-O. Pörtner, D. C. Roberts, V. Masson-Delmotte, P. Zhai, M. Tignor, E. Poloczanska, K. Mintenbeck, A. Alegría, M. Nicolai, A. Okem, J. Petzold, B. Rama, N. M. W) Cambridge University Press (2019).17.Barton, A. D., Irwin, A. J., Finkel, Z. V. & Stock, C. A. Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities. Proc. Natl Acad. Sci. USA 113, 2964–2969 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Pecuchet, L. et al. Spatio‐temporal dynamics of multi‐trophic communities reveal ecosystem‐wide functional reorganization. Ecography 43, 197–208 (2020).Article 

    Google Scholar 
    19.Poloczanska, E. S. et al. Responses of marine organisms to climate change across oceans. Front. Mar. Sci. 3, 62 (2016).20.Pennekamp, F. et al. Biodiversity increases and decreases ecosystem stability. Nature 563, 109–112 (2018).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Duffy, J. E., Godwin, C. M. & Cardinale, B. J. Biodiversity effects in the wild are common and as strong as key drivers of productivity. Nature 549, 261–264 (2017).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    22.Worm, B. et al. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790 (2006).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Blois, J. L., Zarnetske, P. L., Fitzpatrick, M. C. & Finnegan, S. Climate change and the past, present, and future of biotic interactions. Science 341, 499–504 (2013).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Dossena, M. et al. Warming alters community size structure and ecosystem functioning. Proc. R. Soc. B Biol. Sci. 279, 3011–3019 (2012).Article 

    Google Scholar 
    25.Brander, K. & Kiørboe, T. Decreasing phytoplankton size adversely affects ocean food chains. Glob. Chang. Biol. https://doi.org/10.1111/gcb.15216 (2020).26.Mouw, C. B., Barnett, A., McKinley, G. A., Gloege, L. & Pilcher, D. Phytoplankton size impact on export flux in the global ocean. Glob. Biogeochem. Cycles 30, 1542–1562 (2016).ADS 
    CAS 
    Article 

    Google Scholar 
    27.Riahi, K. et al. RCP 8.5—a scenario of comparatively high greenhouse gas emissions. Clim. Change 109, 33–57 (2011).ADS 
    CAS 
    Article 

    Google Scholar 
    28.Magnan, A. K. et al. Implications of the Paris agreement for the ocean. Nat. Clim. Chang. 6, 732–735 (2016).ADS 
    Article 

    Google Scholar 
    29.Kuhn, A. M. et al. Temporal and spatial scales of correlation in marine phytoplankton communities. J. Geophys. Res. Ocean. 124, 9417–9438 (2019).ADS 
    Article 

    Google Scholar 
    30.Sonnewald, M., Dutkiewicz, S., Hill, C. & Forget, G. Elucidating ecological complexity: unsupervised learning determines global marine eco-provinces. Sci. Adv. 6, eaay4740 (2020).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Dutkiewicz, S., Boyd, P. W. & Riebesell, U. Exploring biogeochemical and ecological redundancy in phytoplankton communities in the global ocean. Glob. Chang. Biol. 27, 1196–1213 (2021).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Flombaum, P., Wang, W.-L., Primeau, F. W. & Martiny, A. C. Global picophytoplankton niche partitioning predicts overall positive response to ocean warming. Nat. Geosci. 13, 116–120 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    33.Righetti, D., Vogt, M., Gruber, N., Psomas, A. & Zimmermann, N. E. Global pattern of phytoplankton diversity driven by temperature and environmental variability. Sci. Adv. 5, eaau6253 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    34.Ibarbalz, F. M. et al. Global trends in marine plankton diversity across kingdoms of life. Cell 179, 1084–1097.e21 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    35.Bopp, L. et al. Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences 10, 6225–6245 (2013).ADS 
    Article 

    Google Scholar 
    36.Kwiatkowski, L. et al. Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17, 3439–3470 (2020).ADS 
    CAS 
    Article 

    Google Scholar 
    37.Cabré, A., Marinov, I. & Leung, S. Consistent global responses of marine ecosystems to future climate change across the IPCC AR5 earth system models. Clim. Dyn. 45, 1253–1280 (2015).Article 

    Google Scholar 
    38.Bopp, L., Aumont, O., Cadule, P., Alvain, S. & Gehlen, M. Response of diatoms distribution to global warming and potential implications: a global model study. Geophys. Res. Lett. 32, n/a−n/a (2005).Article 
    CAS 

    Google Scholar 
    39.Dutkiewicz, S. et al. Dimensions of marine phytoplankton diversity. Biogeosciences 17, 609–634 (2020).ADS 
    Article 

    Google Scholar 
    40.Dutkiewicz, S., Scott, J. R. & Follows, M. J. Winners and losers: ecological and biogeochemical changes in a warming ocean. Glob. Biogeochem. Cycles 27, 463–477 (2013).ADS 
    CAS 
    Article 

    Google Scholar 
    41.Marinov, I., Doney, S. C. & Lima, I. D. Response of ocean phytoplankton community structure to climate change over the 21st century: partitioning the effects of nutrients, temperature, and light. Biogeosciences 7, 3941–3959 (2010).ADS 
    Article 

    Google Scholar 
    42.Dutkiewicz, S., Ward, B. A., Scott, J. R. & Follows, M. J. Understanding predicted shifts in diazotroph biogeography using resource competition theory. Biogeosciences 11, 5445–5461 (2014).ADS 
    Article 

    Google Scholar 
    43.Dutkiewicz, S. et al. Impact of ocean acidification on the structure of future phytoplankton communities. Nat. Clim. Chang. 5, 1002–1006 (2015).ADS 
    CAS 
    Article 

    Google Scholar 
    44.Kooijman, S. A. L. M. & Troost, T. A. Quantitative steps in the evolution of metabolic organisation as specified by the dynamic energy budget theory. Biol. Rev. 82, 113–142 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    45.Lévy, M., Jahn, O., Dutkiewicz, S., Follows, M. J. & D’Ovidio, F. The dynamical landscape of marine phytoplankton diversity. J. R. Soc. Interface 12, 20150481 (2015).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Beaugrand, G., Edwards, M., Raybaud, V., Goberville, E. & Kirby, R. R. Future vulnerability of marine biodiversity compared with contemporary and past changes. Nat. Clim. Chang. 5, 695–701 (2015).ADS 
    Article 

    Google Scholar 
    47.Thomas, M. K., Kremer, C. T., Klausmeier, C. A. & Litchman, E. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088 (2012).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Hillebrand, H. et al. Biodiversity change is uncoupled from species richness trends: consequences for conservation and monitoring. J. Appl. Ecol. 55, 169–184 (2018).Article 

    Google Scholar 
    49.Litchman, E. & Klausmeier, C. A. Trait-based community ecology of phytoplankton. Annu. Rev. Ecol. Evol. Syst. 39, 615–639 (2008).Article 

    Google Scholar 
    50.Lindeman, R. L. The trophic-dynamic aspect of ecology. Ecology 23, 399–417 (1942).Article 

    Google Scholar 
    51.Stock, C. A. et al. Reconciling fisheries catch and ocean productivity. Proc. Natl Acad. Sci. USA 114, E1441–E1449 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Armengol, L., Calbet, A., Franchy, G., Rodríguez-Santos, A. & Hernández-León, S. Planktonic food web structure and trophic transfer efficiency along a productivity gradient in the tropical and subtropical Atlantic Ocean. Sci. Rep. 9, 2044 (2019).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    53.Cram, J. A. et al. The role of particle size, ballast, temperature, and oxygen in the sinking flux to the deep sea. Glob. Biogeochem. Cycles 32, 858–876 (2018).ADS 
    CAS 
    Article 

    Google Scholar 
    54.Kéfi, S., Dakos, V., Scheffer, M., Van Nes, E. H. & Rietkerk, M. Early warning signals also precede non-catastrophic transitions. Oikos 122, 641–648 (2013).Article 

    Google Scholar 
    55.Doncaster, C. P. et al. Early warning of critical transitions in biodiversity from compositional disorder. Ecology 97, 3079–3090 (2016).PubMed 
    Article 

    Google Scholar 
    56.Gunderson, L. H. Ecological resilience—in theory and application. Annu. Rev. Ecol. Syst. 31, 425–439 (2000).Article 

    Google Scholar 
    57.Benedetti, F. et al. The seasonal and inter-annual fluctuations of plankton abundance and community structure in a North Atlantic Marine Protected Area. Front. Mar. Sci. 6, 214 (2019).58.Pannard, A., Bormans, M. & Lagadeuc, Y. Short-term variability in physical forcing in temperate reservoirs: effects on phytoplankton dynamics and sedimentary fluxes. Freshw. Biol. 52, 12–27 (2007).CAS 
    Article 

    Google Scholar 
    59.Vidal, T., Calado, A. J., Moita, M. T. & Cunha, M. R. Phytoplankton dynamics in relation to seasonal variability and upwelling and relaxation patterns at the mouth of Ria de Aveiro (West Iberian Margin) over a four-year period. PLoS One 12, e0177237 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    60.Cermeño, P., de Vargas, C., Abrantes, F. & Falkowski, P. G. Phytoplankton biogeography and community stability in the ocean. PLoS One 5, e10037 (2010).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    61.Allen, S. et al. Interannual stability of phytoplankton community composition in the North-East Atlantic. Mar. Ecol. Prog. Ser. 655, 43–57 (2020).ADS 
    Article 

    Google Scholar 
    62.Barton, A. D., Lozier, M. S. & Williams, R. G. Physical controls of variability in North Atlantic phytoplankton communities. Limnol. Oceanogr. 60, 181–197 (2015).ADS 
    Article 

    Google Scholar 
    63.Collins, S., Rost, B. & Rynearson, T. A. Evolutionary potential of marine phytoplankton under ocean acidification. Evol. Appl. 7, 140–155 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    64.Lohbeck, K. T., Riebesell, U. & Reusch, T. B. H. Adaptive evolution of a key phytoplankton species to ocean acidification. Nat. Geosci. 5, 346–351 (2012).ADS 
    CAS 
    Article 

    Google Scholar 
    65.Irwin, A. J., Finkel, Z. V., Müller-Karger, F. E. & Troccoli Ghinaglia, L. Phytoplankton adapt to changing ocean environments. Proc. Natl Acad. Sci. USA 112, 5762–5766 (2015).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Cael, B. B. et al. Marine ecosystem changepoints spread under ocean warming in an Earth System Model. Geophys. Res. Lett.67.Cael, B. B., Dutkiewicz, S. & Henson, S. A. Abrupt shifts in 21st-century plankton communities. Sci. Adv.68.Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).ADS 
    CAS 
    Article 

    Google Scholar 
    69.Burrows, M. T. et al. The pace of shifting climate in marine and terrestrial ecosystems. Science 334, 652–655 (2011).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    70.Chivers, W. J., Walne, A. W. & Hays, G. C. Mismatch between marine plankton range movements and the velocity of climate change. Nat. Commun. 8, 14434 (2017).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    71.Poloczanska, E. S. et al. Global imprint of climate change on marine life. Nat. Clim. Chang. 3, 919–925 (2013).ADS 
    Article 

    Google Scholar 
    72.Jonkers, L., Hillebrand, H. & Kucera, M. Global change drives modern plankton communities away from the pre-industrial state. Nature 570, 372–375 (2019).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    73.Pond, D. W., Tarling, G. A. & Mayor, D. J. Hydrostatic pressure and temperature effects on the membranes of a seasonally migrating marine copepod. PLoS One 9, e111043 (2014).ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    74.Mayor, D. J., Sommer, U., Cook, K. B. & Viant, M. R. The metabolic response of marine copepods to environmental warming and ocean acidification in the absence of food. Sci. Rep. 5, 13690 (2015).ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    75.Richardson, D. M. & Pyšek, P. Elton, C.S. 1958: The ecology of invasions by animals and plants. London: Methuen. Prog. Phys. Geogr. Earth Environ. 31, 659–666 (2007).Article 

    Google Scholar 
    76.May, R. M. Qualitative stability in model ecosystems. Ecology 54, 638–641 (1973).Article 

    Google Scholar 
    77.Lotze, H. K. et al. Global ensemble projections reveal trophic amplification of ocean biomass declines with climate change. Proc. Natl Acad. Sci. USA 116, 12907–12912 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    78.Barange, M. et al. Impacts of climate change on marine ecosystem production in societies dependent on fisheries. Nat. Clim. Chang. 4, 211–216 (2014).ADS 
    Article 

    Google Scholar 
    79.Marañón, E. et al. Unimodal size scaling of phytoplankton growth and the size dependence of nutrient uptake and use. Ecol. Lett. 16, 371–379 (2013).PubMed 
    Article 

    Google Scholar 
    80.Sokolov, A. P. et al. The MIT Integrated Global System Model (IGSM) Version 2: Model Description and Baseline Evaluation Joint Program Report Series, pp. 40 https://globalchange.mit.edu/publication/14579 (2005).81.Dutkiewicz, S. et al. Ocean colour signature of climate change. Nat. Commun. 10, 578 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    82.Monier, E., Scott, J. R., Sokolov, A. P., Forest, C. E. & Schlosser, C. A. An integrated assessment modeling framework for uncertainty studies in global and regional climate change: the MIT IGSM-CAM (version 1.0). Geosci. Model Dev. 6, 2063–2085 (2013).ADS 
    Article 

    Google Scholar 
    83.Moss, R. H. et al. The next generation of scenarios for climate change research and assessment. Nature 463, 747–756 (2010).ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Buitenhuis, E. T. et al. MAREDAT: towards a world atlas of MARine Ecosystem DATa. Earth Syst. Sci. Data 5, 227–239 (2013).ADS 
    Article 

    Google Scholar 
    85.Ward, B. A. Temperature-correlated changes in phytoplankton community structure are restricted to polar waters. PLoS One 10, e0135581 (2015).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    86.Dutkiewicz, S. GUD IGSM depth integrated biomass https://doi.org/10.7910/DVN/LWHQNS (2021).87.Dutkiewicz, S. & Jahn, O. GUD IGSM numerical code and inputs https://doi.org/10.7910/DVN/UA8VNU (2021). More