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      Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades

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          Abstract

          Multiple factors modulate microbial community assembly in the vertebrate gut, though studies disagree as to their relative contribution. One cause may be a reliance on captive animals, which can have very different gut microbiomes compared to their wild counterparts. To resolve this disagreement, we analyze a new, large, and highly diverse animal distal gut 16 S rRNA microbiome dataset, which comprises 80% wild animals and includes members of Mammalia, Aves, Reptilia, Amphibia, and Actinopterygii. We decouple the effects of host evolutionary history and diet on gut microbiome diversity and show that each factor modulates different aspects of diversity. Moreover, we resolve particular microbial taxa associated with host phylogeny or diet and show that Mammalia have a stronger signal of cophylogeny. Finally, we find that environmental filtering and microbe-microbe interactions differ among host clades. These findings provide a robust assessment of the processes driving microbial community assembly in the vertebrate intestine.

          Abstract

          Host phylogeny and diet are major explanatory factors of animal gut microbiome diversity, but our understanding of these associations is limited by a focus on captive animals and a narrow taxonomic scope. Here, the authors isolate evolutionary and ecological drivers of gut microbiomes from wild mammals, birds, reptiles, amphibians, and fish.

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          Most cited references39

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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            PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals

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              Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis.

              Symbiotic bacteria often help their hosts acquire nutrients from their diet, showing trends of co-evolution and independent acquisition by hosts from the same trophic levels. While these trends hint at important roles for biotic factors, the effects of the abiotic environment on symbiotic community composition remain comparably understudied. In this investigation, we examined the influence of abiotic and biotic factors on the gut bacterial communities of fish from different taxa, trophic levels and habitats. Phylogenetic and statistical analyses of 25 16S rRNA libraries revealed that salinity, trophic level and possibly host phylogeny shape the composition of fish gut bacteria. When analysed alongside bacterial communities from other environments, fish gut communities typically clustered with gut communities from mammals and insects. Similar consideration of individual phylotypes (vs. communities) revealed evolutionary ties between fish gut microbes and symbionts of animals, as many of the bacteria from the guts of herbivorous fish were closely related to those from mammals. Our results indicate that fish harbour more specialized gut communities than previously recognized. They also highlight a trend of convergent acquisition of similar bacterial communities by fish and mammals, raising the possibility that fish were the first to evolve symbioses resembling those found among extant gut fermenting mammals. © 2012 Blackwell Publishing Ltd.
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                Author and article information

                Contributors
                nyoungblut@tuebingen.mpg.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                16 May 2019
                16 May 2019
                2019
                : 10
                : 2200
                Affiliations
                [1 ]ISNI 0000 0001 1014 8330, GRID grid.419495.4, Department of Microbiome Science, , Max Planck Institute for Developmental Biology, ; Max Planck Ring 5, 72076 Tübingen, Germany
                [2 ]TU Wien, Institute of Chemical, Environmental and Bioscience Engineering, Research Group for Environmental Microbiology and Molecular Diagnostics 166/5/3, Gumpendorfer Straße 1a, 1060 Vienna, Austria
                [3 ]ISNI 0000 0001 2155 8175, GRID grid.435370.6, ICC Interuniversity Cooperation Centre Water & Health, ; 1160 Vienna, Austria
                [4 ]ISNI 0000 0000 9686 6466, GRID grid.6583.8, Research Institute of Wildlife Ecology, , University of Veterinary Medicine, ; Vienna, 1160 Austria
                [5 ]GRID grid.459693.4, Research Division Water Quality and Health, , Karl Landsteiner University for Health Sciences, ; 3500 Krems an der Donau, Austria
                Author information
                http://orcid.org/0000-0002-3962-8685
                http://orcid.org/0000-0002-0437-5147
                Article
                10191
                10.1038/s41467-019-10191-3
                6522487
                31097702
                3010290d-1122-4fff-8a04-27946760a4af
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 3 December 2018
                : 25 April 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000008, David and Lucile Packard Foundation (David & Lucile Packard Foundation);
                Funded by: Max-Planck-Institut für Entwicklungsbiologie Austrian Science Fund (P23900 & P22032) Niederösterreichische Forschungs- und Bildungsgesellschaft (SC15-016)
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                coevolution,microbial ecology,microbiome,symbiosis
                Uncategorized
                coevolution, microbial ecology, microbiome, symbiosis

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