Captivity humanizes the primate microbiome

Jonathan B. Clayton, Pajau Vangay, Hu Huang, Tonya Ward, Benjamin M. Hillmann, Gabriel A. Al-Ghalith, Dominic A. Travis, Ha Thang Long, Bui Van Tuan, Vo Van Minh, Francis Cabana, Tilo Nadler, Barbara Toddes, Tami Murphy, Kenneth E. Glander, Timothy J. Johnson, Dan Knights

Research output: Contribution to journalArticlepeer-review

166 Scopus citations

Abstract

The primate gastrointestinal tract is home to trillions of bacteria, whose composition is associated with numerous metabolic, autoimmune, and infectious human diseases. Although there is increasing evidence that modern and Westernized societies are associated with dramatic loss of natural human gut microbiome diversity, the causes and consequences of such loss are challenging to study. Here we use nonhuman primates (NHPs) as a model system for studying the effects of emigration and lifestyle disruption on the human gut microbiome. Using 16S rRNA gene sequencing in two model NHP species, we show that although different primate species have distinctive signature microbiota in the wild, in captivity they lose their native microbes and become colonized with Prevotella and Bacteroides, the dominant genera in the modern human gut microbiome. We confirm that captive individuals from eight other NHP species in a different zoo show the same pattern of convergence, and that semicaptive primates housed in a sanctuary represent an intermediate microbiome state between wild and captive. Using deep shotgun sequencing, chemical dietary analysis, and chloroplast relative abundance, we show that decreasing dietary fiber and plant content are associated with the captive primate microbiome. Finally, in a meta-analysis including published human data, we show that captivity has a parallel effect on the NHP gut microbiome to that of Westernization in humans. These results demonstrate that captivity and lifestyle disruption cause primates to lose native microbiota and converge along an axis toward the modern human microbiome.

Original languageEnglish (US)
Pages (from-to)10376-10381
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number37
DOIs
StatePublished - Sep 13 2016

Bibliographical note

Funding Information:
We thank Dr. Michael Murtaugh and Dr. Herbert Covert for critically reading the manuscript and providing feedback; Dr. Lisa Corewyn, Dr. Chris Vinyard, Dr. Susan Williams, Dr. Mark Teaford, and Dr. Marta Salas, who were vital in the collection of individualized fecal samples from the howlers at La Pacifica in Costa Rica; our field assistants, Ai Nguyen Tam and Nguyen Dat, for their help with sample collection and processing in Vietnam; the Endangered Primate Rescue Center, Philadelphia Zoo, Singapore Zoo, and Como Zoo for providing fecal samples from semicaptive and captive nonhuman primates; Tran Van Luong, Nguyen Van Bay, and Nguyen Manh Tien for their permission to work in Son Tra Nature Reserve and for their continued support and help; Kieu Thi Kinh and Thai Van Quang for help in obtaining the research permits; the Department of Forest Protection, the Danang University, and the Son Tra Nature Reserve for granting the research permits; and Christina Valeri and James Collins at the University of Minnesota Veterinary Diagnostic Laboratory for their assistance with acquiring and maintaining shipping permits. This research was funded in part by the Morris Animal Foundation through a Veterinary Student Scholars grant; the University of Minnesota through a College of Veterinary Medicine Travel grant; Merial/NIH through a Summers Scholars grant; the Margot Marsh Biodiversity Foundation; the Mohamed bin Zayed Species Conservation Fund; and the National Institutes of Health through a PharmacoNeuroImmunology Fellowship (NIH/National Institute on Drug Abuse T32 DA007097-32).

Keywords

  • Dietary fiber
  • Dysbiosis
  • Human microbiome
  • Microbial ecology
  • Primate microbiome

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