Within-community variation of interspecific divergence patterns in passerine gut microbiota
Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
35813907
PubMed Central
PMC9251858
DOI
10.1002/ece3.9071
PII: ECE39071
Knihovny.cz E-zdroje
- Klíčová slova
- 16S rRNA, co‐divergence, gut microbiota, metabarcoding, passerines,
- Publikační typ
- časopisecké články MeSH
Gut microbiota (GM) often exhibit variation between different host species and co-divergence with hosts' phylogeny. Identifying these patterns is a key for understanding the mechanisms that shaped symbiosis between GM and its hosts. Therefore, both GM-host species specificity and GM-host co-divergence have been investigated by numerous studies. However, most of them neglected a possibility that different groups of bacteria within GM can vary in the tightness of their association with the host. Consequently, unlike most of these studies, we aimed to directly address how the strength of GM-host species specificity and GM-host co-divergence vary across different GM clades. We decomposed GM communities of 52 passerine species (394 individuals), characterized by 16S rRNA amplicon sequence variant (ASV) profiles, into monophyletic Binned Taxonomic units (BTUs). Subsequently, we analyzed strength of host species specificity and correlation with host phylogeny separately for resulting BTUs. We found that most BTUs exhibited significant host-species specificity in their composition. Notably, BTUs exhibiting high host-species specificity comprised bacterial taxa known to impact host's physiology and immune system. However, BTUs rarely displayed significant co-divergence with host phylogeny, suggesting that passerine GM evolution is not shaped primarily through a shared evolutionary history between the host and its gut microbes.
Department of Zoology Faculty of Science Charles University Prague Czech Republic
Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic
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Bäckhed, F. , Ley, R. E. , Sonnenburg, J. L. , Peterson, D. A. , & Gordon, J. I. (2005). Host‐bacterial mutualism in the human intestine. Science, 307, 1915–1920. PubMed
Balbuena, J. A. , Míguez‐Lozano, R. , & Blasco‐Costa, I. (2013). PACo: A novel Procrustes application to cophylogenetic analysis. PLoS ONE, 8, e61048. PubMed PMC
Balvočiūtė, M. , & Huson, D. H. (2017). SILVA, RDP, Greengenes, NCBI and OTT ‐ how do these taxonomies compare? BMC Genomics, 18, 114. PubMed PMC
Baumann, P. (2005). Biology of bacteriocyte‐associated endosymbionts of plant sap‐sucking insects. Annual Review of Microbiology, 59, 155–189. PubMed
Benjamini, Y. , & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B, 57, 289–300.
Beye, M. , Fahsi, N. , Raoult, D. , & Fournier, P. E. (2018). Careful use of 16S rRNA gene sequence similarity values for the identification of mycobacterium species. New Microbes New Infect, 22, 24–29. PubMed PMC
Bodawatta, K. H. , Klečková, I. , Klečka, J. , Pužejová, K. , Koane, B. , Poulsen, M. , Jønsson, K. A. , & Sam, K. (2022). Specific gut bacterial responses to natural diets of tropical birds. Scientific Reports, 12, 713. PubMed PMC
Bodawatta, K. H. , Koane, B. , Maiah, G. , Sam, K. , Poulsen, M. , & Jønsson, K. A. (2021). Species‐specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight‐associated gut modifications. Proceedings of the Royal Society B: Biological Sciences, 288, rspb.2021.0446. PubMed PMC
Bordenstein, S. R. , & Theis, K. R. (2015). Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biology, 13, e1002226. PubMed PMC
Brooks, A. W. , Kohl, K. D. , Brucker, R. M. , van Opstal, E. J. , & Bordenstein, S. R. (2016). Phylosymbiosis: Relationships and functional effects of microbial communities across host evolutionary history. PLoS Biology, 14, e2000225. PubMed PMC
Brucker, R. M. , & Bordenstein, S. R. (2013). The hologenomic basis of speciation: Gut bacteria cause hybrid lethality in the genus Nasonia. Science, 341, 667–669. PubMed
Callahan, B. J. , McMurdie, P. J. , Rosen, M. J. , Han, A. W. , Johnson, A. J. A. , & Holmes, S. P. (2016). DADA2: High‐resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581–583. PubMed PMC
Capunitan, D. C. , Johnson, O. , Terrill, R. S. , & Hird, S. M. (2020). Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. Molecular Ecology, 29, 829–847. PubMed
Caviedes‐Vidal, E. , McWhorter, T. J. , Lavin, S. R. , Chediack, J. G. , Tracy, C. R. , & Karasov, W. H. (2007). The digestive adaptation of flying vertebrates: High intestinal paracellular absorption compensates for smaller guts. Proceedings of the National Academy of Sciences of the United States of America, 104, 19132–19137. PubMed PMC
Cho, H. , & Lee, W. Y. (2020). Interspecific comparison of the fecal microbiota structure in three Arctic migratory bird species. Ecology and Evolution, 10, 5582–5594. PubMed PMC
Colston, T. J. , & Jackson, C. R. (2016). Microbiome evolution along divergent branches of the vertebrate tree of life: What is known and unknown. Molecular Ecology, 25, 3776–3800. PubMed
Davenport, E. R. (2016). Elucidating the role of the host genome in shaping microbiome composition. Gut Microbes, 7, 178–184. PubMed PMC
Davenport, E. R. , Cusanovich, D. A. , Michelini, K. , Barreiro, L. B. , Ober, C. , & Gilad, Y. (2015). Genome‐wide association studies of the human gut microbiota. PLoS One, 10, 1–22. PubMed PMC
Dewar, M. L. , Arnould, J. P. Y. , Dann, P. , Trathan, P. , Groscolas, R. , & Smith, S. (2013). Interspecific variations in the gastrointestinal microbiota in penguins. Microbiology, 2, 195–204. PubMed PMC
Douglas, A. E. , & Werren, J. H. (2016). Holes in the hologenome: Why host‐microbe symbioses are not holobionts. MBio, 7, 1–7. PubMed PMC
Eckburg, P. B. , Bik, E. M. , Bernstein, C. N. , Purdom, E. , Dethlefsen, L. , Sargent, M. , Gill, S. R. , Nelson, K. E. , & Relman, D. A. (2005). Diversity of the human intestinal microbial flora. Science, 308, 1635–1638. PubMed PMC
Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 26, 2460–2461. PubMed
Falush, D. (2003). Traces of human migrations in helicobacter pylori populations. Science, 299, 1582–1585. PubMed
Gherna, R. L. , Werren, J. H. , Weisburg, W. , Cote, R. , Woese, C. R. , Mandelco, L. , & Brenner, D. J. (1991). Arsenophonus nasoniae gen. Nov., sp. nov., the causative agent of the son‐killer trait in the parasitic wasp Nasonia vitripennis. International Journal of Systematic Bacteriology, 41, 563–565.
Grond, K. , Sandercock, B. K. , Jumpponen, A. , & Zeglin, L. H. (2018). The avian gut microbiota: Community, physiology and function in wild birds. Journal of Avian Biology, 49, 1–19.
Guillot, G. , & Rousset, F. (2013). Dismantling the mantel tests. Methods in ecology and evolution, 4, 336–344.
Harmon, L. J. , & Glor, R. E. (2010). Poor statistical performance of the mantel test in phylogenetic comparative analyses. Evolution, 64, 2173–2178. PubMed
Hedblom, G. A. , Reiland, H. A. , Sylte, M. J. , Johnson, T. J. , & Baumler, D. J. (2018). Segmented filamentous bacteria ‐ metabolism meets immunity. Frontiers in Microbiology, 9, 1–9. PubMed PMC
Heijtz, R. D. , Wang, S. , Anuar, F. , Qian, Y. , Björkholm, B. , Samuelsson, A. , Hibberd, M. L. , Forssberg, H. , & Pettersson, S. (2011). Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences of the United States of America, 108, 3047–3052. PubMed PMC
Hird, S. M. , Sánchez, C. , Carstens, B. C. , & Brumfield, R. T. (2015). Comparative gut microbiota of 59 neotropical bird species. Frontiers in Microbiology, 6, 1–15. PubMed PMC
Hooper, L. V. , Littman, D. R. , & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336, 1268–1273. PubMed PMC
Houtz, J. L. , Sanders, J. G. , Denice, A. , & Moeller, A. H. (2021). Predictable and host‐species specific humanization of the gut microbiota in captive primates. Molecular Ecology, 30, 3667–3687. PubMed PMC
Jami, E. , Israel, A. , Kotser, A. , & Mizrahi, I. (2013). Exploring the bovine rumen bacterial community from birth to adulthood. The ISME Journal, 7, 1069–1079. PubMed PMC
Jetz, W. , Thomas, G. H. , Joy, J. B. , Hartmann, K. , & Mooers, A. O. (2012). The global diversity of birds in space and time. Nature, 491, 444–448. PubMed
Kim, M. , Oh, H. S. , Park, S. C. , & Chun, J. (2014). Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 64, 346–351. PubMed
Klindworth, A. , Pruesse, E. , Schweer, T. , Peplies, J. , Quast, C. , Horn, M. , & Glöckner, F. O. (2013). Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next‐generation sequencing‐based diversity studies. Nucleic Acids Research, 41, 1–11. PubMed PMC
Knutie, S. A. , Wilkinson, C. L. , Kohl, K. D. , & Rohr, J. R. (2017). Early‐life disruption of amphibian microbiota decreases later‐life resistance to parasites. Nature Communications, 8, 86. PubMed PMC
Kropáčková, L. , Těšický, M. , Albrecht, T. , Kubovčiak, J. , Čížková, D. , Tomášek, O. , Martin, J. F. , Bobek, L. , Králová, T. , Procházka, P. , & Kreisinger, J. (2017). Codiversification of gastrointestinal microbiota and phylogeny in passerines is not explained by ecological divergence. Molecular Ecology, 26, 5292–5304. PubMed
Legendre, P. , Oksanen, J. , & ter Braak, C. J. F. (2011). Testing the significance of canonical axes in redundancy analysis. Methods in Ecology and Evolution, 2, 269–277.
Lewis, W. B. , Moore, F. R. , & Wang, S. (2017). Changes in gut microbiota of migratory passerines during stopover after crossing an ecological barrier. Auk, 134, 137–145.
Ley, R. E. , Hamady, M. , Lozupone, C. , Turnbaugh, P. J. , Ramey, R. R. , Bircher, J. S. , Schlegel, M. L. , Tucker, T. A. , Schrenzel, M. D. , Knight, R. , & Gordon, J. I. (2008). Evolution of mammals and their gut microbes. Science, 320, 1647–1651. PubMed PMC
Marietta, E. , Rishi, A. , & Taneja, V. (2015). Immunogenetic control of the intestinal microbiota. Immunology, 145, 313–322. PubMed PMC
McFall‐Ngai, M. , Hadfield, M. G. , Bosch, T. C. G. , Carey, H. V. , Domazet‐Lošo, T. , Douglas, A. E. , Dubilier, N. , Eberl, G. , Fukami, T. , Gilbert, S. F. , Hentschel, U. , King, N. , Kjelleberg, S. , Knoll, A. H. , Kremer, N. , Mazmanian, S. K. , Metcalf, J. L. , Nealson, K. , Pierce, N. E. , … Wernegreen, J. J. (2013). Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America, 110, 3229–3236. PubMed PMC
McMurdie, P. J. , & Holmes, S. (2013). Phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, e61217. PubMed PMC
Moeller, A. H. , Caro‐Quintero, A. , Mjungu, D. , Georgiev, A. V. , Lonsdorf, E. V. , Muller, M. N. , Pusey, A. E. , Peeters, M. , Hahn, B. H. , & Ochman, H. (2016). Cospeciation of gut microbiota with hominids. Science, 353, 380–382. PubMed PMC
Moran, N. A. , & Sloan, D. B. (2015). The Hologenome concept: Helpful or hollow? PLoS Biology, 13, 1–10. PubMed PMC
Moyle, R. G. , Oliveros, C. H. , Andersen, M. J. , Hosner, P. A. , Benz, B. W. , Manthey, J. D. , Travers, S. L. , Brown, R. M. , & Faircloth, B. C. (2016). Tectonic collision and uplift of Wallacea triggered the global songbird radiation. Nature Communications, 7, 1–7. PubMed PMC
Oksanen, J. , Blanchet, F. G. , Kindt, R. , Legendre, P. , Minchin, P. R. , O'Hara, B. , Simpson, G. L. , Solymos, P. , Stevens, H. , & Wagner, H. H. (2016). vegan: Community ecology package.
Paradis, E. , Claude, J. , & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290. PubMed
Parker, B. J. , Hrček, J. , McLean, A. H. C. , & Godfray, A. H. C. J. (2017). Genotype specificity among hosts, pathogens, and beneficial microbes influences the strength of symbiont‐mediated protection. Evolution, 71, 1222–1231. PubMed PMC
Pilchová, T. , Pilet, M. F. , Cappelier, J. M. , Pazlarová, J. , & Tresse, O. (2016). Protective effect of Carnobacterium spp. against listeria monocytogenes during host cell invasion using in vitro HT29 model. Frontiers in Cellular and Infection Microbiology, 6, 1–9. PubMed PMC
Qin, J. , Li, R. , Raes, J. , Arumugam, M. , Burgdorf, K. S. , Manichanh, C. , Nielsen, T. , Pons, N. , Levenez, F. , Yamada, T. , Mende, D. R. , Li, J. , Xu, J. , Li, S. , Li, D. , Cao, J. , Wang, B. , Liang, H. , Zheng, H. , … Wang, J. (2010). A human gut microbial gene catalog established by metagenomic sequencing. Nature, 464, 59–65. PubMed PMC
Quast, C. , Pruesse, E. , Yilmaz, P. , Gerken, J. , Schweer, T. , Yarza, P. , Peplies, J. , & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web‐based tools. Nucleic Acids Research, 41, 590–596. PubMed PMC
R Core Team . (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rognes, T. , Flouri, T. , Nichols, B. , Quince, C. , & Mahé, F. (2016). VSEARCH: A versatile open source tool for metagenomics. PeerJ, 2016, 1–22. PubMed PMC
Rosenberg, E. , & Zilber‐Rosenberg, I. (2011). Symbiosis and development: The hologenome concept. Birth Defects Research Part C: Embryo Today: Reviews, 93, 56–66. PubMed
Rossi‐Tamisier, M. , Benamar, S. , Raoult, D. , & Fournier, P. E. (2015). Cautionary tale of using 16 s rRNA gene sequence similarity values in identification of human‐associated bacterial species. International Journal of Systematic and Evolutionary Microbiology, 65, 1929–1934. PubMed
Sanders, J. G. , Powell, S. , Kronauer, D. J. C. , Vasconcelos, H. L. , Frederickson, M. E. , & Pierce, N. E. (2014). Stability and phylogenetic correlation in gut microbiota: Lessons from ants and apes. Molecular Ecology, 23, 1268–1283. PubMed
Santagati, M. , Campanile, F. , & Stefani, S. (2012). Genomic diversification of enterococci in hosts: The role of the mobilome. Frontiers in Microbiology, 3, 1–9. PubMed PMC
Schliep, K. P. (2011). Phangorn: Phylogenetic analysis in R. Bioinformatics, 27, 592–593. PubMed PMC
Sender, R. , Fuchs, S. , & Milo, R. (2016). Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14, 1–14. PubMed PMC
Sharon, G. , Segal, D. , Ringo, J. M. , Hefetz, A. , Zilber‐Rosenberg, I. , & Rosenberg, E. (2010). Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proceedings of the National Academy of Sciences, 107, 20051–20056. PubMed PMC
Shi, Z. , Zou, J. , Zhang, Z. , Zhao, X. , Noriega, J. , Zhang, B. , Zhao, C. , Ingle, H. , Bittinger, K. , Mattei, L. M. , Pruijssers, A. J. , Plemper, R. K. , Nice, T. J. , Baldridge, M. T. , Dermody, T. S. , Chassaing, B. , & Gewirtz, A. T. (2019). Segmented filamentous bacteria prevent and cure rotavirus infection. Cell, 179, 644–658.e13. PubMed PMC
Solnick, J. V. , & Schauer, D. B. (2001). Emergence of diverse helicobacter species in the pathogenesis of gastric and enterohepatic diseases. Clinical Microbiology Reviews, 14, 59–97. PubMed PMC
Song, S. J. , Sanders, J. G. , Delsuc, F. , Metcalf, J. , Amato, K. , Taylor, M. W. , Mazel, F. , Lutz, H. L. , Winker, K. , Graves, G. R. , Humphrey, G. , Gilbert, J. A. , Hackett, S. J. , White, K. P. , Skeen, H. R. , Kurtis, S. M. , Withrow, J. , Braile, T. , Miller, M. , … Knight, R. (2020). Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. MBio, 11, 1–14. PubMed PMC
Spor, A. , Koren, O. , & Ley, R. (2011). Unravelling the effects of the environment and host genotype on the gut microbiome. Nature Reviews. Microbiology, 9, 279–290. PubMed
Suau, A. , Bonnet, R. , Sutren, M. , Godon, J. J. , Gibson, G. R. , Collins, M. D. , & Doré, J. (1999). Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Applied and Environmental Microbiology, 65, 4799–4807. PubMed PMC
Sullam, K. E. , Essinger, S. D. , Lozupone, C. A. , O'Connor, M. P. , Rosen, G. L. , Knight, R. , Kilham, S. S. , & Russell, J. A. (2012). Environmental and ecological factors that shape the gut bacterial communities of fish: A meta‐analysis. Molecular Ecology, 21, 3363–3378. PubMed PMC
Tannock, G. W. , Miller, J. R. , & Savage, D. C. (1984). Host specificity of filamentous, segmental microorganisms adherent to the small bowel epithelium in mice and rats. Applied and Environmental Microbiology, 47, 441–442. PubMed PMC
Thompson, C. L. , Vier, R. , Mikaelyan, A. , Wienemann, T. , & Brune, A. (2012). “Candidatus Arthromitus” revised: Segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae. Environmental Microbiology, 14, 1454–1465. PubMed
Trevelline, B. K. , Sosa, J. , Hartup, B. K. , & Kohl, K. D. (2020). A bird's‐eye view of phylosymbiosis: Weak signatures of phylosymbiosis among all 15 species of cranes. Proceedings of the Royal Society B: Biological Sciences, 287, 20192988. 10.1098/rspb.2019.2988 PubMed DOI PMC
Waite, D. W. , & Taylor, M. W. (2014). Characterizing the avian gut microbiota: Membership, driving influences, and potential function. Frontiers in Microbiology, 5, 1–12. PubMed PMC
Wang, Q. , Garrity, G. M. , Tiedje, J. M. , & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73, 5261–5267. PubMed PMC
Weiss, B. L. , Maltz, M. , & Aksoy, S. (2012). Obligate symbionts activate immune system development in the tsetse Fly. Journal of Immunology, 188, 3395–3403. PubMed PMC
Wirth, T. , Wang, X. , Linz, B. , Novick, R. P. , Lum, J. K. , Blaser, M. , Morelli, G. , Falush, D. , & Achtman, M. (2004). Distinguishing human ethnic groups by means of sequences from helicobacter pylori: Lessons from Ladakh. Proceedings of the National Academy of Sciences of USA, 101, 4746–4751. PubMed PMC
Wright, E. S. (2015). DECIPHER: Harnessing local sequence context to improve protein multiple sequence alignment. BMC Bioinformatics, 16, 322. PubMed PMC
Yarza, P. , Yilmaz, P. , Pruesse, E. , Glöckner, F. O. , Ludwig, W. , Schleifer, K. H. , Whitman, W. B. , Euzéby, J. , Amann, R. , & Rosselló‐Móra, R. (2014). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nature Reviews. Microbiology, 12, 635–645. PubMed
Youngblut, N. D. , Reischer, G. H. , Walters, W. , Schuster, N. , Walzer, C. , Stalder, G. , Ley, R. E. , & Farnleitner, A. H. (2019). Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nature Communications, 10, 1–15. PubMed PMC
Zilber‐Rosenberg, I. , & Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. FEMS Microbiology Reviews, 32, 723–735. PubMed