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, Tim Johnson, Dan Knights

Research output: Contribution to journalArticle

73 Citations (Scopus)

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

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Microbiota
Primates
Life Style
Prevotella
High-Throughput Nucleotide Sequencing
Bacteroides
Emigration and Immigration
Firearms
Dietary Fiber
Chloroplasts
rRNA Genes
Communicable Diseases
Meta-Analysis
Gastrointestinal Tract
Bacteria
Gastrointestinal Microbiome

Keywords

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

Cite this

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

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 37, 13.09.2016, p. 10376-10381.

Research output: Contribution to journalArticle

Clayton, JB, Vangay, P, Huang, H, Ward, T, Hillmann, BM, Al-Ghalith, GA, Travis, DA, Long, HT, Van Tuan, B, Van Minh, V, Cabana, F, Nadler, T, Toddes, B, Murphy, T, Glander, KE, Johnson, T & Knights, D 2016, 'Captivity humanizes the primate microbiome', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 37, pp. 10376-10381. https://doi.org/10.1073/pnas.1521835113
Clayton, Jonathan B ; Vangay, Pajau ; Huang, Hu ; Ward, Tonya ; Hillmann, Benjamin M. ; Al-Ghalith, Gabriel A. ; Travis, Dominic A ; Long, Ha Thang ; Van Tuan, Bui ; Van Minh, Vo ; Cabana, Francis ; Nadler, Tilo ; Toddes, Barbara ; Murphy, Tami ; Glander, Kenneth E. ; Johnson, Tim ; Knights, Dan. / Captivity humanizes the primate microbiome. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 37. pp. 10376-10381.
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