Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats

ABSTRACT Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from ∼900 vertebrate species, including 315 mammals and 491 birds, assessing...

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Autores principales:	Se Jin Song, Jon G. Sanders, Frédéric Delsuc, Jessica Metcalf, Katherine Amato, Michael W. Taylor, Florent Mazel, Holly L. Lutz, Kevin Winker, Gary R. Graves, Gregory Humphrey, Jack A. Gilbert, Shannon J. Hackett, Kevin P. White, Heather R. Skeen, Sarah M. Kurtis, Jack Withrow, Thomas Braile, Matthew Miller, Kevin G. McCracken, James M. Maley, Vanessa O. Ezenwa, Allison Williams, Jessica M. Blanton, Valerie J. McKenzie, Rob Knight
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	diet evolution flight microbiome vertebrate Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4c88416112104851bafba75448d168c3
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spelling	oai:doaj.org-article:4c88416112104851bafba75448d168c32021-11-15T15:56:58ZComparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats10.1128/mBio.02901-192150-7511https://doaj.org/article/4c88416112104851bafba75448d168c32020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02901-19https://doaj.org/toc/2150-7511ABSTRACT Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from ∼900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Furthermore, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors convergently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome. IMPORTANCE In this comprehensive survey of microbiomes of >900 species, including 315 mammals and 491 birds, we find a striking convergence of the microbiomes of birds and animals that fly. In nonflying mammals, diet and short-term evolutionary relatedness drive the microbiome, and many microbial species are specific to a particular kind of mammal, but flying mammals and birds break this pattern with many microbes shared across different species, with little correlation either with diet or with relatedness of the hosts. This finding suggests that adaptation to flight breaks long-held relationships between hosts and their microbes.Se Jin SongJon G. SandersFrédéric DelsucJessica MetcalfKatherine AmatoMichael W. TaylorFlorent MazelHolly L. LutzKevin WinkerGary R. GravesGregory HumphreyJack A. GilbertShannon J. HackettKevin P. WhiteHeather R. SkeenSarah M. KurtisJack WithrowThomas BraileMatthew MillerKevin G. McCrackenJames M. MaleyVanessa O. EzenwaAllison WilliamsJessica M. BlantonValerie J. McKenzieRob KnightAmerican Society for MicrobiologyarticledietevolutionflightmicrobiomevertebrateMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	diet evolution flight microbiome vertebrate Microbiology QR1-502
spellingShingle	diet evolution flight microbiome vertebrate Microbiology QR1-502 Se Jin Song Jon G. Sanders Frédéric Delsuc Jessica Metcalf Katherine Amato Michael W. Taylor Florent Mazel Holly L. Lutz Kevin Winker Gary R. Graves Gregory Humphrey Jack A. Gilbert Shannon J. Hackett Kevin P. White Heather R. Skeen Sarah M. Kurtis Jack Withrow Thomas Braile Matthew Miller Kevin G. McCracken James M. Maley Vanessa O. Ezenwa Allison Williams Jessica M. Blanton Valerie J. McKenzie Rob Knight Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
description	ABSTRACT Diet and host phylogeny drive the taxonomic and functional contents of the gut microbiome in mammals, yet it is unknown whether these patterns hold across all vertebrate lineages. Here, we assessed gut microbiomes from ∼900 vertebrate species, including 315 mammals and 491 birds, assessing contributions of diet, phylogeny, and physiology to structuring gut microbiomes. In most nonflying mammals, strong correlations exist between microbial community similarity, host diet, and host phylogenetic distance up to the host order level. In birds, by contrast, gut microbiomes are only very weakly correlated to diet or host phylogeny. Furthermore, while most microbes resident in mammalian guts are present in only a restricted taxonomic range of hosts, most microbes recovered from birds show little evidence of host specificity. Notably, among the mammals, bats host especially bird-like gut microbiomes, with little evidence for correlation to host diet or phylogeny. This suggests that host-gut microbiome phylosymbiosis depends on factors convergently absent in birds and bats, potentially associated with physiological adaptations to flight. Our findings expose major variations in the behavior of these important symbioses in endothermic vertebrates and may signal fundamental evolutionary shifts in the cost/benefit framework of the gut microbiome. IMPORTANCE In this comprehensive survey of microbiomes of >900 species, including 315 mammals and 491 birds, we find a striking convergence of the microbiomes of birds and animals that fly. In nonflying mammals, diet and short-term evolutionary relatedness drive the microbiome, and many microbial species are specific to a particular kind of mammal, but flying mammals and birds break this pattern with many microbes shared across different species, with little correlation either with diet or with relatedness of the hosts. This finding suggests that adaptation to flight breaks long-held relationships between hosts and their microbes.
format	article
author	Se Jin Song Jon G. Sanders Frédéric Delsuc Jessica Metcalf Katherine Amato Michael W. Taylor Florent Mazel Holly L. Lutz Kevin Winker Gary R. Graves Gregory Humphrey Jack A. Gilbert Shannon J. Hackett Kevin P. White Heather R. Skeen Sarah M. Kurtis Jack Withrow Thomas Braile Matthew Miller Kevin G. McCracken James M. Maley Vanessa O. Ezenwa Allison Williams Jessica M. Blanton Valerie J. McKenzie Rob Knight
author_facet	Se Jin Song Jon G. Sanders Frédéric Delsuc Jessica Metcalf Katherine Amato Michael W. Taylor Florent Mazel Holly L. Lutz Kevin Winker Gary R. Graves Gregory Humphrey Jack A. Gilbert Shannon J. Hackett Kevin P. White Heather R. Skeen Sarah M. Kurtis Jack Withrow Thomas Braile Matthew Miller Kevin G. McCracken James M. Maley Vanessa O. Ezenwa Allison Williams Jessica M. Blanton Valerie J. McKenzie Rob Knight
author_sort	Se Jin Song
title	Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
title_short	Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
title_full	Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
title_fullStr	Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
title_full_unstemmed	Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats
title_sort	comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/4c88416112104851bafba75448d168c3
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Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats

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