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    Species- and site-specific circulating bacterial DNA in Subantarctic sentinel mussels Aulacomya atra and Mytilus platensis

    Brondizio, E. S., Settele, J., Díaz, S. & Ngo, H. T. (eds.) Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science–Policy Platform on Biodiversity and Ecosystem Services (IPBES Secretariat, 2019).Weiskopf, S. R. et al. Climate change effects on biodiversity, ecosystems, ecosystem services, and natural resource management in the United States. Sci. Total Environ. 733, 137782. https://doi.org/10.1016/j.scitotenv.2020.137782 (2020).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Turner, J. & Marshall, G. J. Climate Change in the Polar Regions (Cambridge University Press, 2011).Book 

    Google Scholar 
    Meredith, M. et al. Polar Regions. Chapter 3, IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. https://www.ipcc.ch/srocc/chapter/chapter-3-2/ (2019).Rignot, E. et al. Four decades of Antarctic Ice Sheet mass balance from 1979–2017. Proc. Natl. Acad. Sci. USA 116, 1095–1103. https://doi.org/10.1073/pnas.1812883116 (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Siegert, M. et al. The Antarctic Peninsula under a 1.5°C global warming scenario. Front. Environ. Sci. 7, 102. https://doi.org/10.3389/fenvs.2019.00102 (2019).Article 

    Google Scholar 
    Iz, H. B. Is the global sea surface temperature rise accelerating?. Geod. Geodyn. 9, 432–438. https://doi.org/10.1016/j.geog.2018.04.002 (2018).Article 

    Google Scholar 
    Qiu, Z. et al. Future climate change is predicted to affect the microbiome and condition of habitat-forming kelp. Proc. R. Soc. B. 286, 20181887. https://doi.org/10.1098/rspb.2018.1887 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Burge, C. A., Kim, C. J., Lyles, J. M. & Harvell, C. D. Special issue Oceans and Humans Health: The ecology of marine opportunists. Microb. Ecol. 65, 869–879. https://doi.org/10.1007/s00248-013-0190-7 (2013).Article 
    PubMed 

    Google Scholar 
    Cavicchioli, R. et al. Scientists’ warning to humanity: Microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586. https://doi.org/10.1038/s41579-019-0222-5 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Harvell, C. D. et al. Emerging marine diseases–climate links and anthropogenic factors. Science 285, 1505–1510. https://doi.org/10.1126/science.285.5433.1505 (1999).CAS 
    Article 
    PubMed 

    Google Scholar 
    Egan, S. & Gardiner, M. Microbial dysbiosis: Rethinking disease in marine ecosystems. Front. Microbiol. 7, 991. https://doi.org/10.3389/fmicb.2016.00991 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wilkins, L. G. E. et al. Host-associated microbiomes drive structure and function of marine ecosystems. PLoS Biol. 17, e3000533. https://doi.org/10.1371/journal.pbio.3000533 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Seuront, L., Nicastro, K. R., Zardi, G. I. & Goberville, E. Decreased thermal tolerance under recurrent heat stress conditions explains summer mass mortality of the blue mussel Mytilus edulis. Sci. Rep. 9, 17498. https://doi.org/10.1038/s41598-019-53580-w (2019).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Tsuchiya, M. Mass mortality in a population of the mussel Mytilus edulis L. caused by high temperature on rocky shores. J. Exp. Mar. Biol. Ecol. 66, 101–111. https://doi.org/10.1016/0022-0981(83)90032-1 (1983).Article 

    Google Scholar 
    Malham, S. K. et al. Summer mortality of the Pacific oyster, Crassostrea gigas, in the Irish Sea: The influence of temperature and nutrients on health and survival. Aquaculture 287, 128–138. https://doi.org/10.1016/j.aquaculture.2008.10.006 (2009).CAS 
    Article 

    Google Scholar 
    Beyer, J. et al. Blue mussels (Mytilus edulis spp.) as sentinel organisms in coastal pollution monitoring: A review. Mar. Environ. Res. 130, 338–365. https://doi.org/10.1016/j.marenvres.2017.07.024 (2017).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Ladeiro, M. P. et al. Mussel as a tool to define continental watershed quality. In Organismal and Molecular Malacology (ed Ray, S.), IntechOpen. https://doi.org/10.5772/67995 (2017).Bonacci, S. et al. Esterase activities in the bivalve mollusc Adamussium colbecki as a biomarker for pollution monitoring in the Antarctic marine environment. Mar. Pollut. Bull. 49, 445–455. https://doi.org/10.1016/j.marpolbul.2004.02.033 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Storhaug, E. et al. Seasonal and spatial variations in biomarker baseline levels within Arctic populations of mussels (Mytilus spp.). Sci. Total Environ. 656, 921–936. https://doi.org/10.1016/j.scitotenv.2018.11.397 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Caza, F. et al. Liquid biopsies for omics-based analysis in sentinel mussels. PLoS ONE 14, e0223525. https://doi.org/10.1371/journal.pone.0225359 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ignatiadis, M., Sledge, G. W. & Jeffrey, S. S. Liquid biopsy enters the clinic – implementation issues and future challenges. Nat. Rev. Clin. Oncol. 18, 297–312. https://doi.org/10.1038/s41571-020-00457-x (2021).Article 
    PubMed 

    Google Scholar 
    Kowarsky, M. et al. Numerous uncharacterized and highly divergent microbes which colonize humans are revealed by circulating cell-free DNA. Proc. Natl. Acad. Sci. USA 114, 9623–9628. https://doi.org/10.1073/pnas.1707009114 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Chen, H. et al. Circulating microbiome DNA: An emerging paradigm for cancer liquid biopsy. Cancer Lett. 521, 82–87. https://doi.org/10.1016/j.canlet.2021.08.036 (2021).CAS 
    Article 
    PubMed 

    Google Scholar 
    Lokmer, A. et al. Spatial and temporal dynamics of Pacific oyster hemolymph microbiota across multiple scales. Front. Microbiol. 7, 1367. https://doi.org/10.3389/fmicb.2016.01367 (2016).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lokmer, A. & Wegner, M. K. Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. ISME J. 9, 670–682. https://doi.org/10.1038/ismej.2014.160 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Auguste, M. et al. Exposure to TiO2 nanoparticles induces shifts in the microbiota composition of Mytilus galloprovincialis hemolymph. Sci. Total Environ. 670, 129–137. https://doi.org/10.1016/j.scitotenv.2019.03.133 (2019).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Vezzulli, L. et al. Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proc. Natl. Acad. Sci. USA 113, E5062–E5071. https://doi.org/10.1073/pnas.1609157113 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Musella, M. et al. Tissue-scale microbiota of the Mediterranean mussel (Mytilus galloprovincialis) and its relationship with the environment. Sci. Total Environ. 717, 137209. https://doi.org/10.1016/j.scitotenv.2020.137209 (2020).ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 
    Féral, J.-P. et al. PROTEKER: Implementation of a submarine observatory at the Kerguelen islands (Southern Ocean). Underw. Technol. 34, 3–10. https://doi.org/10.3723/ut.34.003 (2016).Article 

    Google Scholar 
    Spain, E. A. et al. Shallow seafloor gas emissions near Heard and McDonald Islands on the Kerguelen Plateau, southern Indian Ocean. Earth Space Sci. 7, e2019EA000695. https://doi.org/10.1029/2019EA000695 (2020).ADS 
    Article 

    Google Scholar 
    Cao, S. et al. Structure and function of the Arctic and Antarctic marine microbiota as revealed by metagenomics. Microbiome. 8, 47. https://doi.org/10.1186/s40168-020-00826-9 (2020).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wang, L.-Y. et al. Comparison of bacterial community in aqueous and oil phases of water-flooded petroleum reservoirs using pyrosequencing and clone library approaches. Appl. Microbiol. Biotechnol. 98, 4209–4221. https://doi.org/10.1007/s00253-013-5472-y (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    Gutierrez, T., Berry, D., Teske, A. & Aitken, M. D. Enrichment of Fusobacteria in sea surface oil slicks from the Deepwater Horizon oil spill. Microorganisms. 4, 24. https://doi.org/10.3390/microorganisms4030024 (2016).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    Michelou, V. K., Caporaso, J. G., Knight, R. & Palumbi, S. R. The ecology of microbial communities associated with Macrocystis pyrifera. PLoS ONE 8, e67480. https://doi.org/10.1371/annotation/48e29578-a073-42e7-bca4-2f96a5998374 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Florez, J. Z. et al. Structure of the epiphytic bacterial communities of Macrocystis pyrifera in localities with contrasting nitrogen concentrations and temperature. Algal Res. 44, 101706. https://doi.org/10.1016/j.algal.2019.101706 (2019).Article 

    Google Scholar 
    Minich, J. J. et al. Elevated temperature drives kelp microbiome dysbiosis, while elevated carbon dioxide induces water microbiome disruption. PLoS ONE 13, e0192772. https://doi.org/10.1371/journal.pone.0192772 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Lin, J. D., Lemay, M. A. & Parfrey, L. W. Diverse bacteria utilize alginate within the microbiome of the giant kelp Macrocystis pyrifera. Front. Microbiol. 9, 1914. https://doi.org/10.3389/fmicb.2018.01914 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pierce, M. L. & Ward, J. E. Microbial ecology of the Bivalvia, with an emphasis on the family Ostreidae. J. Shellfish Res. 37, 793–806. https://doi.org/10.2983/035.037.0410 (2018).Article 

    Google Scholar 
    Pierce, M. L. & Ward, J. E. Gut Microbiomes of the Eastern Oyster (Crassostrea virginica) and the Blue Mussel (Mytilus edulis): Temporal variation and the influence of marine aggregate-associated microbial communities. mSphere. 4, e00730-19. https://doi.org/10.1128/mSphere.00730-19 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Delille, D. & Gleizon, F. Distribution of enteric bacteria in Antarctic seawater surrounding the Port-aux-Francais permanent station (Kerguelen Island). Mar. Pollut. Bull. 46, 1179–1183. https://doi.org/10.1016/S0025-326X(03)00164-4 (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    Nguyen, T. V. & Alfaro, A. C. Metabolomics investigation of summer mortality in New Zealand Greenshell mussels (Perna canaliculus). Fish Shellfish Immunol. 106, 783–791. https://doi.org/10.1016/j.fsi.2020.08.022 (2020).CAS 
    Article 
    PubMed 

    Google Scholar 
    Vezzulli, L. et al. Comparative 16SrDNA gene-based microbiota profiles of the Pacific oyster (Crassostrea gigas) and the Mediterranean Mussel (Mytilus galloprovincialis) from a shellfish farm (Ligurian Sea, Italy). Microb. Ecol. 75, 495–504. https://doi.org/10.1007/s00248-017-1051-6 (2018).CAS 
    Article 
    PubMed 

    Google Scholar 
    Romalde, J. L., Diéguez, A. L., Lasa, A. & Balboa, S. New Vibrio species associated to molluscan microbiota: A review. Front. Microbiol. 4, 413. https://doi.org/10.3389/fmicb.2013.00413 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Narayan, N. R. et al. Piphillin predicts metagenomic composition and dynamics from DADA2-corrected 16S rDNA sequences. BMC Genom. 21, 56. https://doi.org/10.1186/s12864-019-6427-1 (2020).CAS 
    Article 

    Google Scholar 
    Peng, W. et al. Integrated 16S rRNA sequencing, metagenomics, and metabolomics to characterize gut microbial composition, function, and fecal metabolic phenotype in non-obese type 2 diabetic Goto-Kakizaki rats. Front. Microbiol. 10, 3141. https://doi.org/10.3389/fmicb.2019.03141 (2020).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Koner, S. et al. Assessment of carbon substrate catabolism pattern and functional metabolic pathway for microbiota of limestone caves. Microorganisms 9, 1789. https://doi.org/10.21203/rs.3.rs-549787/v1 (2021).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Li, Y. F. et al. Temperature elevation and Vibrio cyclitrophicus infection reduce the diversity of haemolymph microbiome of the mussel Mytilus coruscus. Sci. Rep. 9, 16391. https://doi.org/10.1038/s41598-019-52752-y (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Scanes, E. et al. Climate change alters the haemolymph microbiome of oysters. Mar. Pollut. Bull. 164, 111991. https://doi.org/10.1016/j.marpolbul.2021.111991 (2021).CAS 
    Article 
    PubMed 

    Google Scholar 
    Hylander, B. L. & Repasky, E. A. Temperature as a modulator of the gut microbiome: What are the implications and opportunities for thermal medicine?. Int. J. Hyperth. 36, 83–89. https://doi.org/10.1080/02656736.2019.1647356 (2019).CAS 
    Article 

    Google Scholar 
    Lo Giudice, A. et al. Marine bacterioplankton diversity and community composition in an antarctic coastal environment. Microb. Ecol. 63, 210–223. https://doi.org/10.1007/s00248-011-9904-x (2012).Article 
    PubMed 

    Google Scholar 
    Yumoto, I. et al. Temperature and nutrient availability control growth rate and fatty acid composition of facultatively psychrophilic Cobetia marina strain L-2. Arch. Microbiol. 181, 345–351. https://doi.org/10.1007/s00203-004-0662-8 (2004).CAS 
    Article 
    PubMed 

    Google Scholar 
    Weingarten, E. A., Atkinson, C. L. & Jackson, C. R. The gut microbiome of freshwater Unionidae mussels is determined by host species and is selectively retained from filtered seston. PLoS ONE 14, e0224796. https://doi.org/10.1371/journal.pone.0224796 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Rosa, M., Ward, J. E. & Shumway, S. E. Selective capture and ingestion of particles by suspension-feeding bivalve molluscs: A review. J. Shellfish Res. 37, 727–746. https://doi.org/10.2983/035.037.0405 (2018).Article 

    Google Scholar 
    Griffiths, C. L. & King, J. A. Some relationships between size, food availability and energy balance in the ribbed mussel Aulacomya ater. Mar. Biol. 51, 141–149. https://doi.org/10.1007/BF00555193 (1979).Article 

    Google Scholar 
    Riisgård, H. U. Filtration rate and growth in the blue mussel, Mytilus edulis Linneaus, 1758: Dependence on algal concentration. J. Shellfish Res. 10, 29–36 (1991).
    Google Scholar 
    Sonier, R. et al. Picophytoplankton contribution to Mytilus edulis growth in an intensive culture environment. Mar. Biol. 163, 73. https://doi.org/10.1007/s00227-016-2845-7 (2016).Article 

    Google Scholar 
    Jacobs, P., Troost, K., Riegman, R. & Van der Meer, J. Length-and weight-dependent clearance rates of juvenile mussels (Mytilus edulis) on various planktonic prey items. Helgol. Mar. Res. 69, 101–112. https://doi.org/10.1007/s10152-014-0419-y (2015).ADS 
    Article 

    Google Scholar 
    Ward, J. E. & Shumway, S. E. Separating the grain from the chaff: Particle selection in suspension- and deposit-feeding bivalves. J. Exp. Mar. 300, 83–130. https://doi.org/10.1016/j.jembe.2004.03.002 (2004).Article 

    Google Scholar 
    Waite, A. M., Safi, K. A., Hall, J. A. & Nodder, S. D. Mass sedimentation of picoplankton embedded in organic aggregates. Limnol. Oceanogr. 45, 87–97. https://doi.org/10.4319/lo.2000.45.1.0087 (2000).ADS 
    Article 

    Google Scholar 
    Ward, J. E. & Kach, D. J. Marine aggregates facilitate ingestion of nanoparticles by suspension-feeding bivalves. Mar. Environ. Res. 68, 137–142. https://doi.org/10.1016/j.marenvres.2009.05.002 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    Ward, J. E. Biodynamics of suspension-feeding in adult bivalve molluscs: Particle capture, processing, and fate. Invertebr. Biol. 115, 218–231. https://doi.org/10.2307/3226932 (1996).Article 

    Google Scholar 
    Rosa, M. et al. Physicochemical surface properties of microalgae and their combined effects on particle selection by suspension-feeding bivalve molluscs. J. Exp. Mar. 486, 59–68. https://doi.org/10.1016/j.jembe.2016.09.007 (2017).CAS 
    Article 

    Google Scholar 
    Allam, B. & Espinosa, E. P. Bivalve immunity and response to infections: Are we looking at the right place?. Fish Shellfish Immunol. 53, 4–12. https://doi.org/10.1016/j.fsi.2016.03.037 (2016).CAS 
    Article 
    PubMed 

    Google Scholar 
    Barr, J. J. et al. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc. Natl. Acad. Sci. USA 110, 10771–10776. https://doi.org/10.1073/pnas.1305923110 (2013).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Allam, B. & Espinosa, E. P. Mucosal immunity in mollusks. In Mucosal Health in Aquaculture (eds Beck, B. H. & Peatman, E.) 325–370 (Academic Press, 2015).Chapter 

    Google Scholar 
    Huang, J. et al. Hemocytes in the extrapallial space of Pinctada fucata are involved in immunity and biomineralization. Sci. Rep. 8, 4657. https://doi.org/10.1038/s41598-018-22961-y (2018).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kim, H. J. et al. Isolation and characterization of two bacteriophages and their preventive effects against pathogenic Vibrio coralliilyticus causing mortality of Pacific oyster (Crassostrea gigas) larvae. Microorganisms. 8, 926. https://doi.org/10.3390/microorganisms8060926 (2020).CAS 
    Article 
    PubMed Central 

    Google Scholar 
    Ihara, H. et al. Sulfur-oxidizing bacteria mediate microbial community succession and element cycling in launched marine sediment. Front. Microbiol. 8, 152. https://doi.org/10.3389/fmicb.2017.00152 (2017).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Jørgensen, B. B. & Nelson, D. C. Sulfide oxidation in marine sediments: Geochemistry meets microbiology. Geol. S. Am. S. 379, 63–81. https://doi.org/10.1130/0-8137-2379-5.63 (2004).Article 

    Google Scholar 
    Zhou, M. et al. Surface currents and upwelling in Kerguelen Plateau regions. Biogeosci. Discuss. 11, 6845–6876. https://doi.org/10.5194/bgd-11-6845-2014 (2014).ADS 
    Article 

    Google Scholar 
    Gille, S. T., Carranza, M. M., Cambra, R. & Morrow, R. Wind-induced upwelling in the Kerguelen Plateau region. Biogeosciences 11, 6389–6400. https://doi.org/10.5194/bg-11-6389-2014 (2014).ADS 
    Article 

    Google Scholar 
    Park, Y. H., Roquet, F., Durand, I. & Fuda, J. L. Large-scale circulation over and around the Northern Kerguelen Plateau. Deep Sea Res. II(55), 566–581. https://doi.org/10.1016/j.dsr2.2007.12.030 (2008).ADS 
    Article 

    Google Scholar 
    Renac, C. et al. Hydrothermal fluid interaction in basaltic lava units, Kerguelen Archipelago (SW Indian Ocean). Eur. J. 22, 215–234. https://doi.org/10.1127/0935-1221/2009/0022-1993 (2010).CAS 
    Article 

    Google Scholar 
    Vancanneyt, M. et al. Sphingomonas alaskensis sp. nov., a dominant bacterium from a marine oligotrophic environment. Int. J. Syst. Evol. 51, 73–79. https://doi.org/10.1099/00207713-51-1-73 (2001).CAS 
    Article 

    Google Scholar 
    Helmuth, B. S. & Hofmann, G. E. Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol. Bull. 201, 374–384. https://doi.org/10.2307/1543615 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    Testut, L., Wöppelmann, G., Simon, B. & Téchiné, P. The sea level at Port-aux-Français, Kerguelen Island, from 1949 to the present. Ocean Dyn. 56, 464–472. https://doi.org/10.1007/s10236-005-0056-8 (2006).ADS 
    Article 

    Google Scholar 
    Pohl, B. et al. Recent climate variability around the Kerguelen Islands (Southern Ocean) seen through weather regimes. J. Appl. Meteorol. Climatol. 60, 711–731. https://doi.org/10.1175/JAMC-D-20-0255.1 (2021).ADS 
    Article 

    Google Scholar 
    PROTEKER. Ilôt Channer (Passe Royale)—Sea water temperature at 5 and 13 m depth (T°C) daily average 2014–2019. https://www.proteker.net/swt-ilot-channer-passe-royale/ (2021).Caza, F. et al. Comparative analysis of hemocyte properties from Mytilus edulis desolationis and Aulacomya ater in the Kerguelen Islands. Mar. Environ. Res. 110, 174–182. https://doi.org/10.1016/j.marenvres.2015.09.003 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    Caza, F., Cledon, M. & St-Pierre, Y. Biomonitoring climate change and pollution in marine ecosystems: A review on Aulacomya ater. J. Mar. Biol. 2016, 7183813. https://doi.org/10.1155/2016/7183813 (2016).Article 

    Google Scholar 
    Rey-Campos, M. et al. High individual variability in the transcriptomic response of Mediterranean mussels to Vibrio reveals the involvement of myticins in tissue injury. Sci. Rep. 9, 3569. https://doi.org/10.1038/s41598-019-39870-3 (2019).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Caza, F. et al. Hemocytes released in seawater act as Trojan horses for spreading of bacterial infections in mussels. Sci. Rep. 10, 19696. https://doi.org/10.1038/s41598-020-76677-z (2020).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yao, C. L. & Somero, G. N. Thermal stress and cellular signaling processes in hemocytes of native (Mytilus californianus) and invasive (M. galloprovincialis) mussels: Cell cycle regulation and DNA repair. Comp. Biochem. Physiol. 165, 159–168. https://doi.org/10.1016/j.cbpa.2013.02.024 (2013).CAS 
    Article 

    Google Scholar 
    Lockwood, B. L., Sanders, J. G. & Somero, G. N. Transcriptomic responses to heat stress in invasive and native blue mussels (genus Mytilus): Molecular correlates of invasive success. J. Exp. Biol. 213, 3548–3558. https://doi.org/10.1242/jeb.046094 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, e1. https://doi.org/10.1093/nar/gks808 (2013).CAS 
    Article 
    PubMed 

    Google Scholar 
    Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 13, 581–583. https://doi.org/10.1038/nmeth.3869 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2021).
    Google Scholar 
    McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217. https://doi.org/10.1371/journal.pone.0061217 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Oksanen, J. & Blanchet, F. G. Vegan: Community Ecology Package. 2. 3-0 (2015).Ssekagiri, A., Sloan, W. & Ijaz, U. Z. microbiomeSeq: an R package for analysis of microbial communities in an environmental context, In ISCB Africa ASBCB Conference (Kumasi, Ghana, 2017).Cao, Y. Microbiome marker: Microbiome Biomarker Analysis Toolkit. R package version 0.99.0 (2020). https://github.com/yiluheihei/microbiomeMarker. Accessed March 2022.Kanehisa, M. et al. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109–D114. https://doi.org/10.1093/nar/gkr988 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    Iwai, S. et al. Piphillin: Improved prediction of metagenomic content by direct inference from human microbiomes. PLoS ONE 11, e0166104. https://doi.org/10.1371/journal.pone.0166104 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dhariwal, A. et al. MicrobiomeAnalyst: A web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data. Nucleic Acids Res. 45, W180–W188. https://doi.org/10.1093/nar/gkx295 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

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    Attraction to conspecific social-calls in a migratory, solitary, foliage-roosting bat (Lasiurus cinereus)

    Broadcasted social calls attracted hoary bats during both the spring and fall migration. Broadcasting conspecific social calls increased hoary bat capture rates at netting sites intentionally removed from normal capture locations. We had very low capture rates during control periods, because we intentionally placed nets in locations removed from flyways to reduce incidental captures. Moreover, capture rates of hoary bats tend to be low even in many locations where they are known to occur24,25, and capture rates of approximately one bat per hour in a single mist net suggest a very strong attraction response to broadcasted calls.Hoary bat activity, as measured by acoustic monitoring was not associated with increased capture rates in response to call broadcasting. However, subsequent research has shown that hoary bats periodically use higher frequency, inconspicuous calls, or do not constantly echolocate during the fall, which may mean acoustic monitoring did not effectively measure hoary bat activity in the vicinity of our trials26,27. We recorded substantially higher acoustic activity during the spring migration, which could represent either more hoary bats and/or bat activity, or a seasonal difference in echolocation or flight behavior such as differences in flight altitude27. It remains unknown if hoary bats use inconspicuous calls or fly in silence during spring migration or other times of year other than the fall when these inconspicuous echolocation behaviors were observed, and seasonally variable behavior could affect detectability or exposure to our playback trials in ways not captured by our acoustic activity covariate. In addition, while we did audibly hear social calls of hoary bats during the fall, we did not record any during fieldwork for this study, which may be an artifact or due to differences in social behavior, context, or number of hoary bats present in the area during our trials.We only captured one female during trials in New Mexico, and were unable to locate any females during the fall migration in coastal regions of California, despite high concentrations of males in the area during what is presumably the mating season. In New Mexico, during spring migration, females migrate through the study area before males28, with very little temporal overlap. As a result, we were unable to determine sex specific responses to call playback, however we have subsequently captured several female hoary bats and Ope’ape’a (Hawaiian hoary bat, L. semotus) using call playback during capture and radio-tracking studies (GAR, pers. obs.).It is difficult to elucidate the meaning of social calls based on the behaviors observed in the field. In bats, social call complexity often reflects social behavior complexity, with a range of uses including but not limited to attracting mates, locating pups within colonies, defending roosting or foraging territory, and attracting bats to roosts10. Attraction to conspecific call broadcasting could indicate positive social interactions (e.g., maintaining group cohesion or investigation) or agonistic behavior (e.g., hoary bats approaching to chase conspecific bats), as has been observed in other bat species29 and in hoary bats during the maternity season30. We did not observe any obvious instances of aggressive hoary bat interactions, and the social calls differ from hisses and clicks that hoary bats use defensively (Fig. 2). We would also audibly hear pairs of hoary bats calling in close proximity to each other, with no indication of aggressive or territorial responses, and these calls being low frequency and audible to humans means that they attenuate at greater distances than hoary bat echolocation calls.Aggressive or territorial interactions in many taxa are often driven by seasonally variable contexts, such as mating, defending food resources, or rearing of young. It may be unlikely that migrating hoary bats would expend energy defending territory during migration when they are utilizing roosts or foraging habitat for such limited periods of time (i.e., a few hours to a day). During active migration birds are often not territorial even when foraging at stopover sites31, and there may be benefits to maintaining group cohesion during migration including navigation and identification of favorable habitat. It is unknown if hoary bats utilize stopover sites for refueling during migration. However the silver-haired bat Lasionycteris noctivagans was found to utilize a migration stopover site in Long Point, Canada, where they opportunistically foraged for short periods of time (1 to 2 days32). Tracking studies would be required to determine temporal patterns of site usage by individual bats to examine stopover behavior.As we had recorded most of our initial social calls during late summer and early fall when hoary bats mate21, we had originally hypothesized that these social calls were associated with mating behavior, which would have been consistent with observations in this study had we found both increased attraction during the fall, and less attraction to calls during the spring. However, social calls attracted hoary bats effectively during both the spring and fall migration. In addition, from acoustic recordings and capture observations in the field, hoary bats produced many social calls during the spring migration when only males were present. There is a possibility, due to our lack of understanding of the mating systems of hoary bats that some mating may continue into the spring. However the majority of taxonomic, physiological, and observational data suggests mating behavior ends by the spring migration19,33, and the majority of females are already pregnant when travelling through New Mexico28. While hoary bats may or may not use social calls as a component of mating behavior, social calls recorded during the spring likely serve purposes not associated with mating.Previous studies describe the hoary bat as solitary throughout most of the year, which would imply only brief social interactions limited to mating or association with offspring, and the many historical accounts of aggregations of hoary bats are thought to be related to mating behavior20,33,34. However the use of, and attraction to, social calls during both spring and fall migration supports that these calls are used for social interactions beyond mating behavior. Further research may determine if hoary bats use these social calls to maintain group cohesion during migration, and what, if any, relationships exist between individual hoary bats that appear to be migrating together. Baerwald and Barclay35 found that geographic and genetic relationships of hoary bats and silver-haired bat carcasses collected at wind turbines were not more closely related than expected by chance, which provides some evidence that groups of migrating hoary bats may not form based on kinship.Many studies hoping to elucidate the causes of fatalities at wind energy facilities have focused only on the fall migration period when bats are most often killed13,20,36. However hoary bats migrate during the spring as well, when they do not suffer high fatality rates. Investigating the spring migration presents a valuable baseline to compare behavioral changes and other factors that may place hoary bats or other impacted species at risk. If social behavior makes a major contribution to the risk of fatalities at wind energy developments, then social behavior should differ between spring and fall migration. We did not find a large difference in response to social calls between seasons. While this represents just an initial study into the social calling behavior of hoary bats during migration, it provides some conclusions to guide subsequent investigations: (1) detecting hoary bat social calls does not necessarily indicate mating behavior, and (2) researchers should be cautious in interpreting evidence of social interactions during the fall at wind energy sites as evidence of mating behavior as in the mating landmarks hypothesis22,37. Because it can separate out mating from other behavioral components, comparing spring and fall migration can benefit the investigation of social and other behaviors in hoary bats and other migratory species. Comparing flight behavior, diet, roost selection, hormonal and physiological changes, and further studies of social interactions including scent and, between the spring and fall migration will allow researchers to elucidate which behaviors change seasonally and which may underlie seasonal patterns of wind turbine fatalities. Additionally, exploring social attraction to audible sounds produced by turbines or other potential signals that could seasonally elicit social attraction could lead to additional insights.Hoary bats have proven challenging to capture and study in many locations across their range24, driven by their solitary tree roosting behavior and as they often fly out of the reach of mist nets or ground-based acoustic monitoring stations36,38. Using call broadcasting to increase capture rates can be a useful research tool, especially in locations where the habitat does not provide any ideal capture locations. Using this technique we have captured hoary bats on coastal sand dunes, in large open fields, and in groves of Eucalyptus trees adjacent to wind energy sites, all of which would normally yield low bat capture success without the use of lures. The ability to capture hoary bats more reliably is a great asset for research and conservation throughout the range of hoary bats.Our study tested the use of social call playback as a methodology to study the social behavior of hoary bats during migration, and the utility of using call playback as a research tool and acoustic lure for hoary bats. Increasing capture rates from conspecific social call playback during mating and non-mating season indicates social interactions during both migratory periods, despite the solitary roosting behavior of this species. Future studies to elucidate the behavioral function of these calls, and response during non-migratory seasons could refine our understanding of social behaviors of this elusive bat species. 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    CAN-SAR: A database of Canadian species at risk information

    The CAN-SAR22 database was created to provide access to publicly available data on species at risk in Canada in a standardized format that can be used in a wide range of applied research contexts. The variables included in the database were chosen to provide a range of information available for species at risk with a particular focus on climate change to support the first publication using the database6. The database includes numerous data fields including extinction risk status, various biological and geographical attributes, threat assessments, date of listing, recovery actions, and a set of climate change impact and adaptation variables. CAN-SAR is a living database that can be updated as new information and reports become available, or as other targeted data extraction efforts become available23.In Canada, the listing process begins with an assessment of a wildlife species’ risk of extinction by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC). A wildlife species can be either a species or a ‘designatable unit’, which includes subspecies, varieties, or other geographically or genetically distinct populations. Herein these are referred to collectively as ‘species’. COSEWIC is an independent body of experts who synthesize the best available information to date into a status report containing elements such as population size and trends, habitat availability, and threat assessments (Fig. 1)17. This report is then used as the basis for a status recommendation that is passed on to the Government of Canada, who makes the final decision on whether to legally list the species under Schedule 1 of SARA24. The species can be listed as ‘Special concern’, ‘Threatened’, ‘Endangered’, or ‘Extirpated’. If a species is listed as ‘Threatened’, ‘Endangered’ or ‘Extirpated’ then a recovery strategy is required, while for species listed as ‘Special concern’ a management plan must be created24. Recovery strategies must provide a description of the species’ needs, address identified threats, identify critical habitat (where applicable and to the extent possible), and include population and distribution objectives for the species’ recovery. Management plans include conservation measures for the species and its habitat24. Hereafter, we refer to recovery strategies and management plans collectively as ‘recovery documents’.Information included in the database was extracted from various sources and documents that are available from the online SAR Public Registry, including COSEWIC status reports and status appraisal summaries, and recovery documents (Fig. 1). A COSEWIC status appraisal summary is produced instead of a new status report when a species has been previously assessed and COSEWIC experts are confident that its status will not change (https://www.cosewic.ca/index.php/en-ca/assessment-process/status-appraisal-summary-process.html). It is considered an addendum to the existing status report; thus, we use ‘status report’ to refer to either a status report or a status appraisal summary and the previous status report. From the SAR Public Registry website we accessed information from 1146 documents for all 594 species listed under SARA Schedule 1 as of March 23, 2021, that were classified with the status of ‘Special concern’, ‘Threatened’, or ‘Endangered’. Some species have multiple documents of the same type because COSEWIC reassesses at risk species every 10 years or less and recovery strategies and management plans are reviewed every 5 years and updated as needed. As new documents have become available they have been added to the CAN-SAR database without overriding the previously existing document, which allows for tracking of changes in various data fields over time. Only documents between 2018 and 2021, inclusive, have an updated version due to our updating schedule.Data extractionVariables included in the CAN-SAR database were categorised as either directly transcribed or derived. Directly transcribed variables reflect information extracted from documents that require limited interpretation, such as scientific name or date of legal listing (Online-only Table 1). Derived variables reflect species’ attributes that required interpretation of text by data recorders (Online-only Table 1). The data dictionary (CAN-SAR_data_dictionary.xlsx) contains a description of each variable, including details of their extraction and synthesis22.Several derived variables were extracted from the status report technical summary section, including whether the species is endemic to Canada or North America, and whether the species’ range is continuous with the United States. Endemism was determined for each species at two spatial extents, Canada and North America, based on descriptions of their global distributions from status reports. Whether a Canadian species’ range is continuous with its conspecifics in the United States was interpreted from descriptions of geographic isolation in the distribution and rescue effect sections of the status reports.Variables related to species’ threats were derived from information in the status reports, recovery strategies and management plans. In 2012, COSEWIC initiated use of the IUCN threats classification system in status reports for some species; a ‘threats calculator’25. Threats calculators may also be included in recovery strategies and management plans. A threats calculator is a table included in the document that classifies threats into 11 general ‘level one’ classes and, more specific ‘level two’ subclasses (Table 1)26. Four variables (impact, severity, scope, and timing) for each level one and level two threats were scored independently and then combined into an overall impact score for each species. Impact is defined as the degree to which the species is threatened by the threat class; severity is the level of damage to the species from the threat class that is expected within ten years or three generations, whichever is longer; scope is the proportion of the species that is expected to be affected within ten years; and timing is the immediacy of the threat25. Threat-related variables were either transcribed directly from the threats calculator, or from the derived description of threats in the document if a threats calculator was not included.Table 1 Definitions of level one threat classes and names of level two threat classes following Version 1.1 of the IUCN threats classification system.Full size tableFor species where a threats calculator was included, we recorded whether each of the level one and level two threat classes were identified (i.e., considered a threat), and transcribed the scores for each of impact, scope, severity, and timing. Threat classes were considered identified if the impact was negligible, low, moderate, high, very high, unknown, or not calculated (outside assessment timeframe). Impact, scope, severity, and timing values were coded as ranked values of ‘0’: not a threat; ‘1’: neglible; ‘2’: low; ‘3’: moderate; ‘4’: high; ‘5’: very high; ‘-1’: unknown; ‘-2’: not calculated; or ‘NA’ where there were blank values. For exact ranking interpretations see CAN-SAR_data_dictionary22. For some species, the threats calculator was available from the COSEWIC Secretariat as a Microsoft Excel file, in which case threats information was extracted directly from the spreadsheet using R v 3.6.227. For species where a Microsoft Excel file was not available, threats calculator information was manually extracted from the status report.For species where a threats calculator was not included in the document, threats described in the text were classified into threat classes based on version 1.1 of the IUCN threats classification system (Table 1)26. Although a more recent version of the threats calculator exists, we applied version 1.1 classification to reflect the approach applied across the majority of species. Threats were considered identified if the threat was discussed as having any negative or potentially negative impact on the species. In cases where no threat calculator was available, the threat attributes of impact, scope, severity, and timing were scored as not applicable; ‘NA’.Several variables were derived to determine how climate change was addressed in status reports and recovery documents. Whether climate change was mentioned anywhere in the status report was determined by searching the document for the words climat*, warm, temperat*, and drought. If a document contained any of these search terms, we assessed the context for description of anthropogenic climate change impacts. In cases where the terms were not found, the threats section was checked for any other descriptions that were related to climate change; if none were found, climate change was recorded as not mentioned. When climate change was mentioned, we then determined if it was identified as a threat by interpreting whether it was described as having a negative or potentially negative impact on the species. If a threats calculator was included in the status report, climate change was considered a threat if the ‘Climate change and severe weather’ threat class had an impact that was more than negligible or if climate change was described outside the threats calculator as a threat or potential threat. We recorded whether the threat of climate change was unknown. This included instances where climate change was described as having unknown effects on the species, if ‘unknown’ was assigned to impact, scope, severity, or timing in the threats calculator, or if knowledge gaps related to climate change were identified. Finally, the impact of climate change relative to other threats was classified based on descriptions of threats in the status report. The relative impact of climate change was classified as ‘0’ if it was not a threat; ‘1’ if it was described as a minor, potential, possible, or other threat; ‘2’ if it was a significant threat but not the most important or if it was among the list of threats with no indication of relative importance; or ‘3’ if it was among the most important threats described.Additional derived variables extracted from recovery documents available on the SAR Public Registry included those related to critical habitat identification and recovery actions. For species with recovery strategies, we recorded whether critical habitat was described as identified, partially identified, or not identified. In cases where critical habitat was described as “identified to the extent possible”, it was marked as identified. We extracted information from recovery documents on what types of actions were recommended and whether the actions addressed the threat of climate change. Actions were categorized into four categories: outreach and stewardship, research and monitoring, habitat management, and population management (Table 2). Within each of the four categories, a set of 16 sub-types were recorded if any actions of that type were recommended or already completed. We also recorded action types and sub-types that specifically addressed climate change threats if climate change was listed as the threat addressed or the reason the action was necessary6.Table 2 Categories of actions specified in Recovery Strategies.Full size tableFive data recorders conducted the initial data extraction, synthesis, and interpretation. All recorders were trained on the definitions, interpretation, and general process of data extraction to ensure consistent extraction of all variables. Data extraction occurred in multiple stages and included an iterative set of verifications and assessments of the same species among recorders to ensure consistent and standardized interpretations. Once convergence of interpretations was achieved, each recorder was assigned a set of species/reports from which to extract information.Next stepsThe CAN-SAR database is intended to be a living database that can be updated by adding information from new documents or species as they become available, adding more historical documents, or extracting new information from all documents. The current set of species and associated information includes those listed on Schedule 1 of SARA (as of March 23rd 2021) as ‘Special concern’, ‘Threatened’, or ‘Endangered’. Examples of future data additions include integration of data from species assessed by COSEWIC that are not listed under Schedule 1 of SARA, adding fields that specify the criteria used to arrive at a risk status designation, and integration of data from action plans. We anticipate updating the database periodically, as time and resources allow, and we also encourage anyone interested in extending or expanding on the CAN-SAR database to communicate to discuss a collaboration. Integration of new datasets will require screening and validation to ensure adherence to data standards and consistent interpretations. In the longer term, we foresee the implementation of automatic updating of the CAN-SAR database for variables that do not require interpretation by using machine-readable formatted status and recovery documents.ApplicationsApplications of the CAN-SAR database reflect both opportunities to synthesise the data in novel ways and to expand the scope of the current database to include new data fields representing information contained in status assessments and recovery documents. The CAN-SAR database facilitates independent data analysis and synthesis efforts ranging from trend analysis of threats, identifying research and monitoring gaps, and assessing the effectiveness of recovery actions, which target various steps of the listing and recovery process. For example, the database provides a platform to extend existing climate change focused work6 to assess the prevalence of recommended climate change targeted recovery actions, such as translocations. With recent adoption of the ‘Pan-Canadian approach to transforming Species at Risk conservation in Canada’28, which emphasizes multi-species recovery planning approaches, there is an opportunity to assess patterns in key sectors, which include agriculture, forestry, and urban development, over time and by taxa and how they map to threats.With the integration of additional variables through future data extraction or integration efforts, the CAN-SAR database can be used to assess novel questions. For example, broadening recovery action categories to include those that reflect natural climate solutions can highlight where recovery efforts may provide co-benefits, thus achieving biodiversity conservation and climate change mitigation goals29. Specifically, habitat restoration actions for a forest-dependent species primarily threatened by habitat loss may lead to improved recovery outcomes while also resulting in carbon sequestration and improved climate change mitigation efforts. Tracking these types of actions in CAN-SAR could highlight both opportunities and gaps for the integration of climate smart conservation principles30 into species at risk recovery planning and the adoption of climate change adaption measures for species directly considered climate change threatened and those that are not6. More

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    Climate and hydraulic traits interact to set thresholds for liana viability

    TRY meta-­analysisWe used the TRY plant trait database27 to identify traits that show systematic differences between the tree and liana growth forms, as a way to narrow the scope of the rest of the analysis. We chose traits to represent major trade­offs within the “economic spectrum” framework, which places plants along a spectrum of strategies from acquisitive, fast return on investment to conservative, slow return on investment according to key functional trait values30. We narrowed traits to those that had observations for at least four tree and liana species. We then compiled our dataset using the following steps during November and December 2019. For each trait, we downloaded the dataset for all species available globally and averaged the observations of the trait to the species level to avoid statistical biases introduced in our growth form comparison due to a high density of observations in a few commercially valuable species. We matched the species ID number with the most frequently used growth form identifier using the TRY “growth form” trait and kept the species with the most frequent identifier of “tree,” “liana,” or “woody vine.” We subsetted the data to keep only species with a majority of observations ascribed to the tree and liana growth forms (i.e., no herbaceous species, ferns, etc.), resulting in observations for 44,222 total species. Finally, we filtered the dataset of 44,222 species by hand to remove species misclassified as trees or lianas; species occurring entirely in temperate to boreal biomes; species from all gymnosperm lineages except the order Gnetales; and entries for taxonomic classifications broader than the genus level (e.g., taxonomic families). We found that hydraulic functional traits in the TRY database (i.e., Ks,max and P50) show systematic differences between growth forms (Supplementary Fig. 1; Supplementary Tables 3 and 4), while there is mixed evidence for differences in the acquisitiveness of trees and lianas in terms of stem anatomical traits (Supplementary Fig. 1; Supplementary Tables 3 and 4) and leaf functional traits (Supplementary Fig. 6; Supplementary Tables 3 and 4), and no evidence of differences between tropical trees and lianas with respect to root functional traits (Supplementary Fig. 7; Supplementary Tables 3 and 4).Extended meta­-analysisWe conducted an additional literature search to supplement the hydraulic trait observations from the TRY database. The additional literature search served two purposes: (1) to fill a major gap identified during our TRY analysis in terms of liana trait observations, and (2) to address the methodological inconsistency of measuring Ks,max and P50 on liana branches shorter than the longest vessel, which incorrectly measures Ks,max and P50 without accounting for end wall resistivity59,60.We conducted a literature search using Web of Science and Google Scholar. We searched the following phrases in combination with “liana:” “hydraulic conductivity,” “hydraulic trait,” “hydraulic efficiency,” and “hydraulic K.” Of the literature we found, we kept only the studies that met the following criteria: (1) reported Ks,max measurements for lianas, (2) measured Ks,max instead of computing Ks,max from xylem conduit dimensions, (3) measured Ks,max on sunlit, terminal branches of mature individuals or saplings, and (4) measured Ks,max on a branch longer than the longest vessel. We considered the authors to have used a branch length longer than maximum vessel length if the authors measured or reported maximum vessel length for the species and a longer branch was used. Because the best methodological practice for measuring P50, especially in species with long vessels, is currently a matter of debate, we additionally removed all observations of P50  > ­0.75. This filtering was performed to reduce the probability that falsely high (i.e., less negative) P50 values were retained in our analysis because of improper measurement technique and is consistent with the P50 filtering performed by Trugman et al.61. Improper measurement technique is a particular concern for lianas, whose wide and long vessels require cautious implementation of the traditional measurement techniques developed for trees. We note that retaining all liana P50 observations (i.e., not filtering out observations  > −0.75) results in a significant difference between trees and lianas (Mann­–Whitney test statistic = 1029, ntree = 61, nliana = 46, p  More

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    Enhancing soil quality makes crop production more resilient to climate change

    Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.This is a summary of: Qiao, L. et al. Soil quality both increases crop production and improves resilience to climate change. Nat. Clim. Change https://doi.org/10.1038/s41558-022-01376-8 (2022). More

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    DNA databases of an important tropical timber tree species Shorea leprosula (Dipterocarpaceae) for forensic timber identification

    cpDNA haplotype databaseDNA sequencing of the choloroplast (cp) markers produced sequences of the following lengths: 573 bp (atpB-rbcL); 487 bp (petG-trnP); 500 bp (trnL1-trnL2); and 593 bp (psbM-trnD). Alignment of the 352 individuals from the 44 populations yielded a total 28 variable sites: 11 in the atpB-rbcL spacer, seven in both the petG-trnP and psbM-trnD spacers, and three in the trnL1-trnL2 spacer (Supplementary Table S1). Based on these 28 variable sites (21 base substitutions and 7 deletions) across the combined intergenic regions, a total of 22 unique haplotypes were found (Fig. 1a).Figure 1(a) Chloroplast haplotype distribution in the Shorea leprosula populations. The pie chart colours indicate haplotype distributions; and sector areas are proportional to sample size (Map was generated by ArcGIS-ArcMap version 10.8). (b) STRUCTURE analysis identified two clusters (K = 2) corresponding to Region A and B.Full size imageSSR allele frequency databaseThe reproducibility of SSR genotyping was confirmed by achieving consistent genotypes from five independent PCR amplifications on a single individual for each of the ten SSR loci. Individual bar plots from STRUCTURE analysis are presented in Fig. 1b. At the highest Delta K likelihood scores, the best representation of the data was K = 2 suggesting that the 44 populations in Peninsular Malaysia can be divided into two main genetic clusters: Region A and Region B. The first cluster, ‘Region A’ consists of 12 populations, namely SBadak, BPerangin, BEnggang, GJerai, RTelui, GInas, GBongsu, Belum, Piah, BHijau, Korbu and Bubu. The second cluster, ‘Region B’ consists of 32 populations, namely Behrang, Ampang, HGombak, HLangat, SLalang, PPanjang, Berembun, Angsi, Kenaboi, Triang, Pasoh, BSenggeh, GLedang, Krau, TNegara, Terenggun, SBetis, USat, CTongkat, HTerengganu, Jengai, AGading, Tekam, Beserah, Jengka, Lentang, Lesong, ERompin, GArong, Labis, AHitam and Panti. Similarly, the UPGMA dendrogram analysis also divided the 44 populations into two genetic clusters (Fig. 2) corresponding to Region A and B of the STRUCTURE result.Figure 2Dendrogram showing the relationship between 44 populations of Shorea leprosula in Peninsular Malaysia based on the UPGMA cluster analysis of SSR markers.Full size imageSSR allele frequency databases were established according to Region A and B, and characterized to evaluate the relative usefulness of each SSR marker in forensic investigation. The distribution of allele frequencies for each locus is listed in Table S2 (Region A database) and Table S3 (Region B database). Forensic parameters are shown in Table 1, with a total of 143 alleles and 174 alleles detected in the Region A and B databases, respectively. The observed (Ho) and expected (He) heterozygosity ranged from 0.3570 to 0.8346 and 0.4375 to 0.8795, respectively for populations in the Region A database; and ranged from 0.3298 to 0.8356 and 0.3469 to 0.8793, respectively for populations in the Region B database. The power of discrimination (PD) for the SSR loci ranged from 0.601 to 0.972 and 0.554 to 0.975, in Region A and B databases, respectively. The most discriminating locus was Sle605 in both the Region A (PD = 0.972) and Region B (PD = 0.975) databases. Minimum allele frequency was adjusted for alleles falling below the thresholds of 0.0066 (Region A) and 0.0024 (Region B).Table 1 Genetic diversity and forensic variables (A: total number of alleles; Ho: observed heterozygosity; He: expected heterozygosity; PIC: polymorphic information content; HWE: Hardy–Weinberg equilibrium; MP: matching probability; PD: power of discrimination) for each the 10 SSR loci of Shorea leprosula in the Region A and B databases.Full size tableDeviations from HWE were detected in four of the SSR loci for Region A (SleT11, SleT15, SleT17 and Sle465) and six SSR loci in Region B (SleT01, SleT11, SleT15, SleT17, SleT29 and SleT31). We evaluated these loci in each population independently to rule out the possible presence of null alleles. There were four populations in Region A (GJerai, RTelui, GBongsu and Piah) where a single one locus deviated from HWE; whereas there were eight populations in Region B (Behrang, HGombak, SLalang, Angsi, Klau, USat, Jengka and Panti) with a single locus and a single population (GLedang) with two loci that deviated from HWE (Table S4). Observed deviation from HWE was substantially lower in each population (either absence or not more than two loci) and thus it might be due to Wahlund effect caused by population substructuring in both Region A and B. Linkage disequilibrium (LD) testing was used to evaluate the independence of frequencies for all the SSR genotypes. A total of 13.3% and 28.9% of the 45 pairwise loci were found significant evidence of LD for Region A and B, respectively. Some of the loci might be linked as a result of population substructuring and inbreeding (inbreeding coefficient = 0.0822 [Peninsular Malaysia]). These results are in line with observations in real populations, where the assumption of completely random mating and zero migration required for HWE and LD are unlikely to be met, either in humans, animals or plants 21,22,23.Mean self-assignment, the proportion of individuals correctly assigned back to their population, was 45.9% and ranged from 14.3% (Kenaboi) to 81.3% (CTongkat) between population (Table 2). At the regional level, correct assignment rate of individuals to their region of origin was higher, 87.4% for Region A and 90.0% for Region B, (average of 88.7%).Table 2 Self-assignment test outcomes for Shorea leprosula individuals at the population and regional levels.Full size tableConservativeness of the databaseThe coancestry coefficient (θ) for Peninsular Malaysia (0.0579) was higher than those of Region A (0.0454) and Region B (0.0500) (Table 3). A total of 4.54% and 5.00% of the genetic variability was distributed among populations within Region A and Region B, respectively. In terms of inbreeding coefficient (f), the value for the Region A database (f = 0.0892) was highest, followed by Peninsular Malaysia (f = 0.0822) and Region B (f = 0.0666). All the θ and f values were significantly greater than zero, demonstrated by the 95% confidence intervals not overlapping with zero. Both of the θ and f values were used to calculate the conservativeness of each database by testing the cognate database (Porigin) against the regional database (Pcombined). The databases were non-conservative at the calculated θ value. In order for both the Region databases (A and B) to be conservative, the value of θ was adjusted from 0.0454 to 0.1900 for Region A and from 0.0500 to 0.1500 for Region B. For the Region A database, the most common SSR profile frequency is 2.69 × 10–7 or 1 in 3.72 million and the rarest profile frequency is 1.84 × 10–14 or 1 in 54.3 trillion. For the Region B database, the most common SSR profile frequency is 1.06 × 10–7 or 1 in 9.43 million and the rarest profile frequency is 4.03 × 10–16 or 1 in 2.48 quadrillion.Table 3 Coancestry (θ) and inbreeding (f) coefficients for Shorea leprosula at each hierarchical level.Full size table More

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    A catastrophic collapse for the ‘flying banana’ of the Kalahari

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    Identification of nosZ-expressing microorganisms consuming trace N2O in microaerobic chemostat consortia dominated by an uncultured Burkholderiales

    Montzka SA, Dlugokencky EJ, Butler JH. Non-CO2 greenhouse gases and climate change. Nature 2011;476:43–50.CAS 
    PubMed 
    Article 

    Google Scholar 
    Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, et al. (eds). Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press; 2021. (in press).Wuebbles DJ. Nitrous oxide: no laughing matter. Science. 2009;326:56–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kool DM, Dolfing J, Wrage N, van Groenigen JW. Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol Biochem. 2011;43:174–8.CAS 
    Article 

    Google Scholar 
    Yoon S, Song B, Phillips RL, Chang J, Song MJ. Ecological and physiological implications of nitrogen oxide reduction pathways on greenhouse gas emissions in agroecosystems. FEMS Microbiol Ecol. 2019;95:fiz066.CAS 
    PubMed 
    Article 

    Google Scholar 
    Sanford RA, Wagner DD, Wu Q, Chee-Sanford JC, Thomas SH, Cruz-García C, et al. Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci USA. 2012;109:19709–14.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hallin S, Philippot L, Löffler FE, Sanford RA, Jones CM. Genomics and ecology of novel N2O-reducing microorganisms. Trends Microbiol. 2018;26:43–55.CAS 
    PubMed 
    Article 

    Google Scholar 
    Graf DR, Jones CM, Hallin S. Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions. PLoS One. 2014;9:e114118.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Roco CA, Bergaust LL, Bakken LR, Yavitt JB, Shapleigh JP. Modularity of nitrogen‐oxide reducing soil bacteria: linking phenotype to genotype. Environ Microbiol. 2017;19:2507–19.CAS 
    PubMed 
    Article 

    Google Scholar 
    Jones CM, Graf DR, Bru D, Philippot L, Hallin S. The unaccounted yet abundant nitrous oxide-reducing microbial community: A potential nitrous oxide sink. ISME J. 2013;7:417–26.CAS 
    PubMed 
    Article 

    Google Scholar 
    Frostegård Å, Vick SH, Lim NY, Bakken LR, Shapleigh JP. Linking meta-omics to the kinetics of denitrification intermediates reveals pH-dependent causes of N2O emissions and nitrite accumulation in soil. ISME J. 2022;16:26–37.PubMed 
    Article 
    CAS 

    Google Scholar 
    Simon J, Einsle O, Kroneck PMH, Zumft WG. The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase. FEBS Lett. 2004;569:7–12.CAS 
    PubMed 
    Article 

    Google Scholar 
    Foley J, De Haas D, Yuan Z, Lant P. Nitrous oxide generation in full-scale biological nutrient removal wastewater treatment plants. Water Res. 2010;44:831–44.CAS 
    PubMed 
    Article 

    Google Scholar 
    Zheng J, Doskey PV. Simulated rainfall on agricultural soil reveals enzymatic regulation of short-term nitrous oxide profiles in soil gas and emissions from the surface. Biogeochemistry. 2016;128:327–38.CAS 
    Article 

    Google Scholar 
    Kern M, Simon J. Three transcription regulators of the Nss family mediate the adaptive response induced by nitrate, nitric oxide or nitrous oxide in Wolinella succinogenes. Environ Microbiol. 2016;18:2899–912.CAS 
    PubMed 
    Article 

    Google Scholar 
    Suenaga T, Riya S, Hosomi M, Terada A. Biokinetic characterization and activities of N2O-reducing bacteria in response to various oxygen levels. Front Microbiol. 2018;9:697.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kim DD, Park D, Yoon H, Yun T, Song MJ, Yoon S. Quantification of nosZ genes and transcripts in activated sludge microbiomes with novel group-specific qPCR methods validated with metagenomic analyses. Water Res. 2020;185:116261.CAS 
    PubMed 
    Article 

    Google Scholar 
    Yoon S, Nissen S, Park D, Sanford RA, Löffler FE. Nitrous oxide reduction kinetics distinguish bacteria harboring clade I NosZ from those harboring clade II NosZ. Appl Environ Microbiol. 2016;82:3793–800.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yoon H, Song MJ, Kim DD, Sabba F, Yoon S. A serial biofiltration system for effective removal of low-concentration nitrous oxide in oxic gas streams: mathematical modeling of reactor performance and experimental validation. Environ Sci Technol. 2019;53:2063–74.CAS 
    PubMed 
    Article 

    Google Scholar 
    Suenaga T, Hori T, Riya S, Hosomi M, Smets BF, Terada A. Enrichment, isolation, and characterization of high-affinity N2O-reducing bacteria in a gas-permeable membrane reactor. Environ Sci Technol. 2019;53:12101–12.CAS 
    PubMed 
    Article 

    Google Scholar 
    Conthe M, Wittorf L, Kuenen JG, Kleerebezem R, van Loosdrecht MC, Hallin S. Life on N2O: Deciphering the ecophysiology of N2O respiring bacterial communities in a continuous culture. ISME J. 2018;12:1142–53.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Henry S, Bru D, Stres B, Hallet S, Philippot L. Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol. 2006;72:5181–9.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Qi C, Zhou Y, Suenaga T, Oba K, Lu J, Wang G, et al. Organic carbon determines nitrous oxide consumption activity of clade I and II nosZ bacteria: Genomic and biokinetic insights. Water Res. 2022;209:117910.CAS 
    Article 

    Google Scholar 
    Gao Y, Mania D, Mousavi SA, Lycus P, Arntzen MØ, Woliy K, et al. Competition for electrons favours N2O reduction in denitrifying Bradyrhizobium isolates. Environ Microbiol. 2021;23:2244–59.CAS 
    PubMed 
    Article 

    Google Scholar 
    Song MJ, Choi S, Bae WB, Lee J, Han H, Kim DD, et al. Identification of primary effecters of N2O emissions from full-scale biological nitrogen removal systems using random forest approach. Water Res. 2020;184:116144.CAS 
    PubMed 
    Article 

    Google Scholar 
    Ahn JH, Kim S, Park H, Rahm B, Pagilla K, Chandran K. N2O emissions from activated sludge processes, 2008−2009: results of a national monitoring survey in the United States. Environ Sci Technol. 2010;44:4505–11.CAS 
    PubMed 
    Article 

    Google Scholar 
    Bollmann A, Conrad R. Influence of O2 availability on NO and N2O release by nitrification and denitrification in soils. Glob Chang Biol 1998;4:387–96.Article 

    Google Scholar 
    Morris RL, Schmidt TM. Shallow breathing: Bacterial life at low O2. Nat Rev Microbiol. 2013;11:205–12.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Marchant HK, Ahmerkamp S, Lavik G, Tegetmeyer HE, Graf J, Klatt JM, et al. Denitrifying community in coastal sediments performs aerobic and anaerobic respiration simultaneously. ISME J. 2017;11:1799–812.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Camejo PY, Oyserman BO, McMahon KD, Noguera DR. Integrated omic analyses provide evidence that a “Candidatus Accumulibacter phosphatis” strain performs denitrification under microaerobic conditions. mSystems. 2019;4:e00193–18.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Yoon S, Sanford RA, Löffler FE. Shewanella spp. use acetate as an electron donor for denitrification but not ferric iron or fumarate reduction. Appl Environ Microbiol. 2013;79:2818–22.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    van den Berg EM, Boleij M, Kuenen JG, Kleerebezem R, van Loosdrecht M. DNRA and denitrification coexist over a broad range of acetate/N-NO3− ratios, in a chemostat enrichment culture. Front Microbiol. 2016;7:1842.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Sander R. Compilation of Henry’s law constants (version 4.0) for water as solvent. Atmos Chem Phys. 2015;15:4399–981.CAS 
    Article 

    Google Scholar 
    Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME2. Nat Biotechnol. 2019;37:852–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Binder BJ, Liu YC. Growth rate regulation of rRNA content of a marine Synechococcus (cyanobacterium) strain. Appl Environ Microbiol. 1998;64:3346–51.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Shrestha PM, Rotaru AE, Aklujkar M, Liu F, Shrestha M, Summers ZM, et al. Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ Microbiol Rep. 2013;5:904–10.CAS 
    PubMed 
    Article 

    Google Scholar 
    Ritalahti KM, Amos BK, Sung Y, Wu Q, Koenigsberg SS, Löffler FE. Quantitative PCR targeting 16S rRNA and reductive dehalogenase genes simultaneously monitors multiple Dehalococcoides strains. Appl Environ Microbiol. 2006;72:2765–74.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    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 
    Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: A new versatile metagenomic assembler. Genome Res. 2017;27:824–34.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Hyatt D, Chen G-L, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: Prokaryotic gene recognition and translation initiation site identification. BMC Bioinform. 2010;11:1–11.Article 
    CAS 

    Google Scholar 
    Buchfink B, Reuter K, Drost H-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021;18:366–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428:726–31.CAS 
    PubMed 
    Article 

    Google Scholar 
    Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–97.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–13.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Huang Y, Gilna P, Li W. Identification of ribosomal RNA genes in metagenomic fragments. Bioinformatics 2009;25:1338–40.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Miller CS, Baker BJ, Thomas BC, Singer SW, Banfield JF. EMIRGE: reconstruction of full-length ribosomal genes from microbial community short read sequencing data. Genome Biol. 2011;12:R44.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–6.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint arXiv:13033997. 2013.Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009;25:2078–9.PubMed 
    PubMed Central 

    Google Scholar 
    Quinlan AR, Hall IM. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 2010;26:841–2.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Nayfach S, Pollard KS. Toward accurate and quantitative comparative metagenomics. Cell 2016;166:1103–16.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011;12:1–16.Article 

    Google Scholar 
    Li D, Liu C-M, Luo R, Sadakane K, Lam T-W. MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 2015;31:1674–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 2015;3:e1165.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ, Evans PN, et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2017;2:1533–42.CAS 
    PubMed 
    Article 

    Google Scholar 
    Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Olm MR, Brown CT, Brooks B, Banfield JF. dRep: A tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 2017;11:2864–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rodriguez-R LM, Gunturu S, Harvey WT, Rosselló-Mora R, Tiedje JM, Cole JR, et al. The Microbial Genomes Atlas (MiGA) webserver: taxonomic and gene diversity analysis of Archaea and Bacteria at the whole genome level. Nucleic Acids Res. 2018;46:W282–8.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Darling AE, Jospin G, Lowe E, Matsen FA IV, Bik HM, Eisen JA. PhyloSift: Phylogenetic analysis of genomes and metagenomes. PeerJ. 2014;2:e243.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol. 2007;56:564–77.CAS 
    PubMed 
    Article 

    Google Scholar 
    Salazar G, Paoli L, Alberti A, Huerta-Cepas J, Ruscheweyh H-J, Cuenca M, et al. Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell 2019;179:1068–83.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Milanese A, Mende DR, Paoli L, Salazar G, Ruscheweyh H-J, Cuenca M, et al. Microbial abundance, activity and population genomic profiling with mOTUs2. Nat Commun. 2019;10:1014.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Sunagawa S, Mende DR, Zeller G, Izquierdo-Carrasco F, Berger SA, Kultima JR, et al. Metagenomic species profiling using universal phylogenetic marker genes. Nat Methods. 2013;10:1196–9.CAS 
    PubMed 
    Article 

    Google Scholar 
    Yap CX, Henders AK, Alvares GA, Wood DL, Krause L, Tyson GW, et al. Autism-related dietary preferences mediate autism-gut microbiome associations. Cell 2021;184:5916–31.CAS 
    PubMed 
    Article 

    Google Scholar 
    Shan J, Sanford RA, Chee‐Sanford J, Ooi SK, Löffler FE, Konstantinidis KT, et al. Beyond denitrification: the role of microbial diversity in controlling nitrous oxide reduction and soil nitrous oxide emissions. Glob Chang Biol. 2021;27:2669–83.PubMed 
    Article 

    Google Scholar 
    Jones CM, Spor A, Brennan FP, Breuil M-C, Bru D, Lemanceau P, et al. Recently identified microbial guild mediates soil N2O sink capacity. Nat Clim Chang. 2014;4:801–5.Kim J, Kim DD, Yoon S. Rapid isolation of fast-growing methanotrophs from environmental samples using continuous cultivation with gradually increased dilution rates. Appl Microbiol Biotechnol. 2018;102:5707–15.CAS 
    PubMed 
    Article 

    Google Scholar 
    Betlach MR, Tiedje JM. Kinetic explanation for accumulation of nitrite, nitric oxide, and nitrous oxide during bacterial denitrification. Appl Environ Microbiol. 1981;42:1074–84.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Bueno E, Mesa S, Bedmar EJ, Richardson DJ, Delgado MJ. Bacterial adaptation of respiration from oxic to microoxic and anoxic conditions: Redox control. Antioxid Redox Signal. 2012;16:819–52.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Rauhamäki V, Bloch DA, Wikström M. Mechanistic stoichiometry of proton translocation by cytochrome cbb3. Proc Natl Acad Sci USA. 2012;109:7286–91.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Borisov VB, Gennis RB, Hemp J, Verkhovsky MI. The cytochrome bd respiratory oxygen reductases. Biochim Biophys Acta – Bioenerg. 2011;1807:1398–413.CAS 
    Article 

    Google Scholar 
    Lee A, Winther M, Priemé A, Blunier T, Christensen S. Hot spots of N2O emission move with the seasonally mobile oxic-anoxic interface in drained organic soils. Soil Biol Biochem. 2017;115:178–86.CAS 
    Article 

    Google Scholar 
    Orellana L, Rodriguez-R L, Higgins S, Chee-Sanford J, Sanford R, Ritalahti K, et al. Detecting nitrous oxide reductase (nosZ) genes in soil metagenomes: method development and implications for the nitrogen cycle. MBio 2014;5:e01193–14.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Ormeño-Orrillo E, Martínez-Romero E. A genomotaxonomy view of the Bradyrhizobium genus. Front Microbiol. 2019;10:1334.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Tong W, Li X, Wang E, Cao Y, Chen W, Tao S, et al. Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts. BMC Genom. 2020;21:186.CAS 
    Article 

    Google Scholar 
    Conthe M, Lycus P, Arntzen MØ, da Silva AR, Frostegård Å, Bakken LR, et al. Denitrification as an N2O sink. Water Res. 2019;151:381–7.CAS 
    PubMed 
    Article 

    Google Scholar 
    Goldblatt C, Lenton TM, Watson AJ. Bistability of atmospheric oxygen and the Great Oxidation. Nature. 2006;443:683–6.CAS 
    PubMed 
    Article 

    Google Scholar 
    Brewer PG, Hofmann AF, Peltzer ET, Ussler W III. Evaluating microbial chemical choices: The ocean chemistry basis for the competition between use of O2 or NO3− as an electron acceptor. Deep Sea Res Part I Oceanogr Res Pap. 2014;87:35–42.CAS 
    Article 

    Google Scholar 
    Bianchi D, Dunne JP, Sarmiento JL, Galbraith ED. Data‐based estimates of suboxia, denitrification, and N2O production in the ocean and their sensitivities to dissolved O2. Global Biogeochem Cycles 2012;26:GB2009.Stolper DA, Revsbech NP, Canfield DE. Aerobic growth at nanomolar oxygen concentrations. Proc Natl Acad Sci USA. 2010;107:18755–60.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    Zakem E, Follows M. A theoretical basis for a nanomolar critical oxygen concentration. Limnol Oceanogr. 2017;62:795–805.Article 

    Google Scholar 
    Liengaard L, Nielsen LP, Revsbech NP, Priemé A, Elberling B, Enrich-Prast A, et al. Extreme emission of N2O from tropical wetland soil (Pantanal, South America). Front Microbiol. 2013;3:433.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    Shcherbak I, Robertson GP. Nitrous oxide (N2O) emissions from subsurface soils of agricultural ecosystems. Ecosystems. 2019;22:1650–63.CAS 
    Article 

    Google Scholar 
    Qu Z, Bakken LR, Molstad L, Frostegård Å, Bergaust LL. Transcriptional and metabolic regulation of denitrification in Paracoccus denitrificans allows low but significant activity of nitrous oxide reductase under oxic conditions. Environ Microbiol. 2016;18:2951–63.CAS 
    PubMed 
    Article 

    Google Scholar 
    Desloover J, Roobroeck D, Heylen K, Puig S, Boeckx P, Verstraete W, et al. Pathway of nitrous oxide consumption in isolated Pseudomonas stutzeri strains under anoxic and oxic conditions. Environ Microbiol. 2014;16:3143–52.CAS 
    PubMed 
    Article 

    Google Scholar  More