TY - JOUR
T1 - Captivity humanizes the primate microbiome
AU - Clayton, Jonathan B.
AU - Vangay, Pajau
AU - Huang, Hu
AU - Ward, Tonya
AU - Hillmann, Benjamin M.
AU - Al-Ghalith, Gabriel A.
AU - Travis, Dominic A.
AU - Long, Ha Thang
AU - Van Tuan, Bui
AU - Van Minh, Vo
AU - Cabana, Francis
AU - Nadler, Tilo
AU - Toddes, Barbara
AU - Murphy, Tami
AU - Glander, Kenneth E.
AU - Johnson, Timothy J.
AU - Knights, Dan
PY - 2016/9/13
Y1 - 2016/9/13
N2 - 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.
AB - 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.
KW - Dietary fiber
KW - Dysbiosis
KW - Human microbiome
KW - Microbial ecology
KW - Primate microbiome
UR - http://www.scopus.com/inward/record.url?scp=84987602243&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84987602243&partnerID=8YFLogxK
U2 - 10.1073/pnas.1521835113
DO - 10.1073/pnas.1521835113
M3 - Article
C2 - 27573830
AN - SCOPUS:84987602243
VL - 113
SP - 10376
EP - 10381
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 37
ER -