Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.)
The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between host...
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Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 118; no. 47; pp. 1 - 9 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
National Academy of Sciences
23.11.2021
|
Series | From the Cover |
Subjects | |
Online Access | Get full text |
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Abstract | The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts. |
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AbstractList | The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts. Understanding the factors that sculpt gut microbial communities in mammals is of great interest. Here, we studied a diverse clade of herbivorous rodents (woodrats, Neotoma ) with variable but well-characterized diets and habitats to quantify the relative contributions of host genetics, geography, and diet, alongside neutral processes, in structuring the gut microbiome under natural and controlled conditions. While diet and geography made significant contributions to microbiome structure, host phylogeny explained the greatest proportion of observed variation. Provision of a common diet in captivity altered natural microbial communities, with communities from different species varying in their resistance to this perturbation. Captivity increased the amount of variation explained by host phylogeny, further emphasizing the extent to which host genetics structure mammalian microbiomes. The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma , we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts. The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus , we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts. |
Author | Dearing, M. Denise Greenhalgh, Robert Dale, Colin Stapleton, Tess E. Kohl, Kevin D. Orr, Teri J. Weinsteina, Sara B. Martínez-Mota, Rodolfo Klure, Dylan M. |
Author_xml | – sequence: 1 givenname: Sara B. surname: Weinsteina fullname: Weinsteina, Sara B. – sequence: 2 givenname: Rodolfo surname: Martínez-Mota fullname: Martínez-Mota, Rodolfo – sequence: 3 givenname: Tess E. surname: Stapleton fullname: Stapleton, Tess E. – sequence: 4 givenname: Dylan M. surname: Klure fullname: Klure, Dylan M. – sequence: 5 givenname: Robert surname: Greenhalgh fullname: Greenhalgh, Robert – sequence: 6 givenname: Teri J. surname: Orr fullname: Orr, Teri J. – sequence: 7 givenname: Colin surname: Dale fullname: Dale, Colin – sequence: 8 givenname: Kevin D. surname: Kohl fullname: Kohl, Kevin D. – sequence: 9 givenname: M. Denise surname: Dearing fullname: Dearing, M. Denise |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34799446$$D View this record in MEDLINE/PubMed |
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Keywords | 16S rRNA neutral model DNA metabarcoding Neotoma phylosymbiosis |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions: S.B.W., C.D., K.D.K., and M.D.D. designed research; S.B.W., R.M.-M., T.E.S., D.M.K., and T.J.O. performed research; R.G. contributed new reagents/analytic tools; S.B.W., D.M.K., and R.G. analyzed data; and S.B.W., C.D., K.D.K., and M.D.D. wrote the paper. Edited by Margaret McFall-Ngai, University of Hawaii at Manoa, Honolulu, HI, and approved October 19, 2021 (received for review May 11, 2021) |
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Snippet | The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence... Understanding the factors that sculpt gut microbial communities in mammals is of great interest. Here, we studied a diverse clade of herbivorous rodents... |
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SubjectTerms | Animals Animals, Wild - microbiology Bacteria - classification Bacteria - genetics Biological Sciences Captivity Composition Diet Genetics Geography Intestinal microflora Microbiomes Microbiota Microorganisms Neotoma Phylogeny RNA, Ribosomal, 16S Sigmodontinae - microbiology Southwestern United States Species Specificity Structural stability Symbionts Symbiosis Toxins Wild animals |
Title | Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats (Neotoma spp.) |
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