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Primate phageomes are structured by superhost phylogeny and environment.

Publication ,  Journal Article
Gogarten, JF; Rühlemann, M; Archie, E; Tung, J; Akoua-Koffi, C; Bang, C; Deschner, T; Muyembe-Tamfun, J-J; Robbins, MM; Schubert, G; Surbeck, M ...
Published in: Proceedings of the National Academy of Sciences of the United States of America
April 2021

Humans harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. These gut bacterial communities in turn host diverse bacteriophage (hereafter phage) communities that have a major impact on their structure, function, and, ultimately, human health. However, the evolutionary and ecological origins of these human-associated phage communities are poorly understood. To address this question, we examined fecal phageomes of 23 wild nonhuman primate taxa, including multiple representatives of all the major primate radiations. We find relatives of the majority of human-associated phages in wild primates. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost codivergence is often detected for individual phages. Within species, neighboring social groups harbor compositionally and evolutionarily distinct phageomes, which are structured by superhost social behavior. Captive nonhuman primate phageome composition is intermediate between that of their wild counterparts and humans. Phage phylogenies reveal replacement of wild great ape-associated phages with human-associated ones in captivity and, surprisingly, show no signal for the persistence of wild-associated phages in captivity. Together, our results suggest that potentially labile primate-phage associations have persisted across millions of years of evolution. Across primates, these phylosymbiotic and sometimes codiverging phage communities are shaped by transmission between groupmates through grooming and are dramatically modified when primates are moved into captivity.

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Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

April 2021

Volume

118

Issue

15

Start / End Page

e2013535118

Related Subject Headings

  • Virome
  • Social Behavior
  • Phylogeny
  • Hominidae
  • Gastrointestinal Microbiome
  • Evolution, Molecular
  • Environment
  • Bacteriophages
  • Animals
 

Citation

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Gogarten, J. F., Rühlemann, M., Archie, E., Tung, J., Akoua-Koffi, C., Bang, C., … Calvignac-Spencer, S. (2021). Primate phageomes are structured by superhost phylogeny and environment. Proceedings of the National Academy of Sciences of the United States of America, 118(15), e2013535118. https://doi.org/10.1073/pnas.2013535118
Gogarten, Jan F., Malte Rühlemann, Elizabeth Archie, Jenny Tung, Chantal Akoua-Koffi, Corinna Bang, Tobias Deschner, et al. “Primate phageomes are structured by superhost phylogeny and environment.Proceedings of the National Academy of Sciences of the United States of America 118, no. 15 (April 2021): e2013535118. https://doi.org/10.1073/pnas.2013535118.
Gogarten JF, Rühlemann M, Archie E, Tung J, Akoua-Koffi C, Bang C, et al. Primate phageomes are structured by superhost phylogeny and environment. Proceedings of the National Academy of Sciences of the United States of America. 2021 Apr;118(15):e2013535118.
Gogarten, Jan F., et al. “Primate phageomes are structured by superhost phylogeny and environment.Proceedings of the National Academy of Sciences of the United States of America, vol. 118, no. 15, Apr. 2021, p. e2013535118. Epmc, doi:10.1073/pnas.2013535118.
Gogarten JF, Rühlemann M, Archie E, Tung J, Akoua-Koffi C, Bang C, Deschner T, Muyembe-Tamfun J-J, Robbins MM, Schubert G, Surbeck M, Wittig RM, Zuberbühler K, Baines JF, Franke A, Leendertz FH, Calvignac-Spencer S. Primate phageomes are structured by superhost phylogeny and environment. Proceedings of the National Academy of Sciences of the United States of America. 2021 Apr;118(15):e2013535118.
Journal cover image

Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

April 2021

Volume

118

Issue

15

Start / End Page

e2013535118

Related Subject Headings

  • Virome
  • Social Behavior
  • Phylogeny
  • Hominidae
  • Gastrointestinal Microbiome
  • Evolution, Molecular
  • Environment
  • Bacteriophages
  • Animals