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Microbiomes of microscopic marine invertebrates do not reveal signatures of phylosymbiosis

  • Gilbert, S. F., Sapp, J. & Tauber, A. I. A symbiotic view of life: we have never been individuals. Q. Rev. Biol. 87, 325–341 (2012).

    PubMed 
    Article 

    Google Scholar 

  • Bass, D., Stentiford, G. D., Wang, H.-C., Koskella, B. & Tyler, C. R. The pathobiome in animal and plant diseases. Trends Ecol. Evol. 34, 996–1008 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Husnik, F. & Keeling, P. J. The fate of obligate endosymbionts: reduction, integration, or extinction. Curr. Opin. Genet. Dev. 58-59, 1–8 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Berg, G. et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome 8, 103 (2020).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Kwong, W. K. & Moran, N. A. Gut microbial communities of social bees. Nat. Rev. Microbiol. 14, 374–384 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Hammer, T. J., Janzen, D. H., Hallwachs, W., Jaffe, S. P. & Fierer, N. Caterpillars lack a resident gut microbiome. Proc. Nat Acad. Sci. USA 114, 9641–9646 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Holt, C. C., van der Giezen, M., Daniels, C. L., Stentiford, G. D. & Bass, D. Spatial and temporal axes impact ecology of the gut microbiome in juvenile European lobster (Homarus gammarus). ISME J. 14, 531–543 (2020).

    PubMed 
    Article 

    Google Scholar 

  • Pollock, F. J. et al. Coral-associated bacteria demonstrate phylosymbiosis and cophylogeny. Nat. Commun. 9, 4921 (2018).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Thomas, T. et al. Diversity, structure and convergent evolution of the global sponge microbiome. Nat. Commun. 7, 11870 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Engelberts, J. P. et al. Characterization of a sponge microbiome using an integrative genome-centric approach. ISME J. 14, 1100–1110 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Mallot, E. K. & Amato, K. R. Host specificity of the gut microbiome. Nat. Rev. Microbiol. 19, 639–653 (2021).

    Article 
    CAS 

    Google Scholar 

  • Colston, T. J. & Jackson, C. R. Microbiome evolution along divergent branches of the vertebrate tree of life: what is known and unknown. Mol. Ecol. 25, 3776–3800 (2016).

    PubMed 
    Article 

    Google Scholar 

  • Levin, D. et al. Diversity and functional landscapes in the microbiota of animals in the wild. Science 372, eabb5352 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Nishida, A. H. & Ochman, H. Rates of gut microbiome divergence in mammals. Mol. Ecol. 27, 1884–1897 (2013).

    Article 

    Google Scholar 

  • Brooks, A. W., Kohl, K. D., Brucker, R. M., van Opstal, E. J. & Bordenstein, S. R. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 14, e2000225 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Mazel, F. et al. Is host filtering the main driver of phylosymbiosis across the tree of life? mSystems 3, https://doi.org/10.1128/mSystems.00097-18 (2018).

  • Lutz, H. L. et al. Ecology and host identity outweigh evolutionary history in shaping the bat microbiome. mBio 4, 6 (2019).

    Google Scholar 

  • Grond, K. et al. No evidence for phylosymbiosis in Western chipmunk species. FEMS Microbiol. Ecol. 96, fiz182 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Song, S. J. et al. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio 11, 1 (2020).

    Article 

    Google Scholar 

  • Trevelline, B. K., Sosa, J., Hartup, B. K. & Kohl, K. D. A bird’s-eye view of phylosymbiosis: weak signatures of phylosymbiosis among all 15 species of cranes. Proc. R. Soc. B 287, 20192988 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Youngblut, N. D. et al. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat. Commun. 10, 2200 (2019).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Amato, K. R. et al. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J. 13, 576–587 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Moeller, A. H. et al. Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2, e1500997 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Eckert, E. M., Anicic, N. & Fontaneto, D. Freshwater zooplankton microbiome composition is highly flexible and strongly influenced by the environment. Mol. Ecol. 30, 1545–1558 (2021).

    PubMed 
    Article 

    Google Scholar 

  • Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–228 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bik, H. M. Microbial metazoa are microbes too. mSystems 4, e00109–e00119 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Schuelke, T., Pereira, T. J., Hardy, S. M. & Bik, H. M. Nematode-associated microbial taxa do not correlate with host phylogeny, geographic region or feeding morphology in marine sediment habitats. Mol. Ecol. 27, 1930–1951 (2018).

    PubMed 
    Article 

    Google Scholar 

  • Guidetti, R. et al. Further insights in the Tardigrada microbiome: phylogenetic position and prevalence of infection of four new Alphaproteobacteria putative endosymbionts. Zool. J. Linn. Soc. 188, 925–937 (2020).

    Article 

    Google Scholar 

  • Giere, O. Meiobenthology (Springer-Verlag, 2009).

  • Laumer, C. E. et al. Revisiting metazoan phylogeny with genomic sampling of all phyla. Proc. R. Soc. B 286, 20190831 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Hammer, T. J., Sanders, J. G. & Fierer, N. Not all animals need a microbiome. FEMS Microbiol. Lett. 366, fnz117 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Alejandre-Colomo, C. et al. Cultivable Winogradskyella species are genomically distinct from the sympatric abundant candidate species. ISME Commun. 1, 51 (2021).

    Article 

    Google Scholar 

  • Husnik, F. et al. Bacterial and archaeal symbioses with protists. Curr. Biol. 31, R862–R877 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Salje, J. Cells within cells: Rickettsiales and the obligate intracellular bacterial lifestyle. Nat. Rev. Microbiol. 19, 375–390 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Neave, M. J., Apprill, A., Ferrier-Pagès, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315–8324 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Weiland-Bräuer, N. et al. Composition of bacterial communities associated with Aurelia aurita changes with compartment, life stage, and population. Appl. Environ. Microbiol. 81, 6038–6052 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Bik, E. M. et al. Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat. Commun. 7, 10516 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Burns, A. R. et al. Contribution of neutral processes to the assembly of gut microbial communities in the zebrafish over host development. ISME J. 10, 655–664 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • McFall-Ngai, M. Adaptive immunity: care for the community. Nature 445, 153 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Ruehland, C. & Dubilier, N. Gamma- and epsilonproteobacterial ectosymbionts of a shallow-water marine worm are related to deep-sea hydrothermal vent ectosymbionts. Environ. Microbiol. 12, 2312–2326 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Gruber-Vodicka, H. R. et al. Two intracellular and cell-type specific bacterial symbionts in the placozoan Trichoplax H2. Nat. Microbiol. 4, 1465–1474 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Schockaert, E. R. in Methods for the Examination of Organismal Diversity in Soils and Sediments (ed. Hall, G. S.) 211–225 (CABI, 1996).

  • Higgins, R. P. in Introduction to the Study of Meiofauna (eds. Higgins, R. P. and Thiel, H.) 328–331 (SIP, 1988).

  • Schram, M. D. & Davison, P. G. Irwin Loops—a history and method of constructing homemade loops. Trans. Kans. Acad. Sci. 115, 35–40 (1903).

    Article 

    Google Scholar 

  • Medlin, L., Elwood, H. J., Stickel, S. & Sogin, M. L. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491–499 (1988).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Bower, S. M. et al. Preferential PCR amplification of parasitic protistan small subunit rDNA from metazoan tissues. J. Eukaryot. Microbiol. 51, 325–332 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Comeau, A. M., Li, W. K. W., Tremblay, J.-E., Carmack, E. C. & Lovejoy, C. Arctic ocean microbial community structure before and after the 2007 record sea ice minimum. PLoS ONE 6, e27492 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Zhang, R.-Y. et al. Design of targeted primers based on 16S rRNA sequences in meta-transcriptomic datasets and identification of a novel taxonomic group in the Asgard archaea. BMC Microbiol. 20, 25 (2020).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Lane, D. J. in Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. & Goodfellow, M) 115–175 (Wiley, 1991).

  • Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Marcel, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 17, 10 (2011).

    Google Scholar 

  • R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2020).

  • Callahan, B. J. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    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 (2013).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6, 226 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2016).

  • Love, M. I., Huber, W. & Anders, S. Moderate estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

  • Kurtz, Z. D. Sparse and compositionally robust inference of microbial ecological networks. PLoS Comput. Biol. 11, e1004226 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • Csardi, G. & Nepusz, T. The igraph Software Package for Complex Network Research (InterJournal, 2006).

  • Breiman, L. Random forests. Mach. Learn. 45, 5–32 (2001).

  • Kolde, R. pheatmap: pretty heatmaps. R package version 1.0.12 https://CRAN.R-project.org/package=pheatmap (2015).

  • Lin, H. & Das Peddada, S. Analysis of composition of microbiomes with bias correction. Nat. Commun. 11, 3514 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Oksanen, J. vegan: Community Ecology Package. R package version 2.5.7 https://CRAN.R-project.org/package=vegan (2020).

  • Rouse, G., Pleijel, F. & Tilic, E. Annelida (Oxford Univ. Press, 2022).

  • Ahmed, M. & Holovachov, O. Twenty years after De Ley and Blaxter—How far did we progress in understanding the phylogeny of the phylum Nematoda? Animals 11, 3479 (2021).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Van Steenkiste, N. W. L., Herbert, E. R. & Leander, B. S. Species diversity in the marine microturbellarian Astrotorhynchus bifidus sensu lato (Platyhelminthes: Rhabdocoela) from the Northeast Pacific Ocean. Mol. Phylogenet. Evol. 120, 259–273 (2018).

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