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Edited by James J. Bull, University of Idaho, Moscow, ID, and approved February 24, 2021 (received for review July 1, 2020)
Significance
Mammals harbor diverse communities of gut microbes. The assembly and evolution of the bacterial components of these communities are influenced by host evolutionary histories and social behavior. Little is known about the ecological and evolutionary origins of the phages infecting these bacteria. We explore drivers of phage community assembly and phage lineage evolution in primates. Many phages codiverged with their superhosts. Furthermore, neighboring social groups harbor compositionally and evolutionary distinct phageomes, structured by superhost social behavior. Captive primate phageome composition is intermediate to humans and their wild primate counterparts, with phage phylogenies revealing replacement of wild-associated phages by human-associated lineages. This plasticity makes the long-term associations of phages with their superhosts observed across ecosystems and continents all the more striking.
Abstract
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.
Footnotes
- ↵1To whom correspondence may be addressed. Email: jan.gogarten{at}gmail.com or calvignacs{at}rki.de.
Author contributions: J.F.G., J.F.B., A.F., F.H.L., and S.C.-S. designed research; J.F.G., M.R., E.A., J.T., C.A.-K., C.B., T.D., J.-J.M.-T., M.M.R., G.S., M.S., R.M.W., K.Z., F.H.L., and S.C.-S. performed research; J.F.G. and M.R. analyzed data; and J.F.G., M.R., E.A., J.T., C.A.-K., C.B., T.D., J.-J.M.-T., M.M.R., G.S., M.S., R.M.W., K.Z., J.F.B., A.F., F.H.L., and S.C.-S. wrote the paper.
The authors declare no competing interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2013535118/-/DCSupplemental.
Data Availability
The data supporting the conclusions of this article are available in the supporting information, with the exception of the larger files that are available through the Zenodo open-access repository (https://zenodo.org/record/4641870). Code for quality control and assembly of contigs is available here: https://github.com/mruehlemann/metagenome_preproc/blob/master/qc_and_assemble.slurm. All sequences generated as part of this study have been uploaded to the project accession number PRJNA692042. Data from previously published work are available through project accession number PRJNA271618 and ERP104379.
Published under the PNAS license.
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Primate phageomes are structured by superhost phylogeny and environment
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