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Proc Natl Acad Sci U S A. 2016 Sep 13;113(37):10376-81. doi: 10.1073/pnas.1521835113. Epub 2016 Aug 29.

Captivity humanizes the primate microbiome.

Author information

1
Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, MN 55108; GreenViet Biodiversity Conservation Center, Danang 59000, Vietnam;
2
Bioinformatics and Computational Biology, University of Minnesota, Minneapolis, MN 55455;
3
Biotechnology Institute, University of Minnesota, Saint Paul, MN 55108;
4
Department of Computer Science and Engineering, University of Minnesota, Minneapolis, MN 55455;
5
Department of Veterinary Population Medicine, University of Minnesota, Saint Paul, MN 55108;
6
GreenViet Biodiversity Conservation Center, Danang 59000, Vietnam; Frankfurt Zoological Society, 60316 Frankfurt, Germany;
7
GreenViet Biodiversity Conservation Center, Danang 59000, Vietnam;
8
Department of Environment and Biology, Danang University of Education, Danang 59000, Vietnam;
9
Wildlife Nutrition Centre, Wildlife Reserves Singapore, 729826, Singapore;
10
Endangered Primate Rescue Center, Cuc Phuong National Park, Nho Quan, Ninh BÌnh, 40000, Vietnam;
11
Philadelphia Zoological Garden, Philadelphia, PA 19108;
12
Como Park Zoo & Conservatory, Saint Paul, MN 55103;
13
Department of Evolutionary Anthropology, Duke University, Durham, NC 27708.
14
Department of Veterinary and Biomedical Sciences, University of Minnesota, Saint Paul, MN 55108;
15
Biotechnology Institute, University of Minnesota, Saint Paul, MN 55108; Department of Computer Science and Engineering, University of Minnesota, Minneapolis, MN 55455; dknights@umn.edu.

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.

KEYWORDS:

dietary fiber; dysbiosis; human microbiome; microbial ecology; primate microbiome

PMID:
27573830
PMCID:
PMC5027417
DOI:
10.1073/pnas.1521835113
[Indexed for MEDLINE]
Free PMC Article

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