Literature DB >> 27573830

Captivity humanizes the primate microbiome.

Jonathan B Clayton1, Pajau Vangay2, Hu Huang2, Tonya Ward3, Benjamin M Hillmann4, Gabriel A Al-Ghalith2, Dominic A Travis5, Ha Thang Long6, Bui Van Tuan7, Vo Van Minh8, Francis Cabana9, Tilo Nadler10, Barbara Toddes11, Tami Murphy12, Kenneth E Glander13, Timothy J Johnson14, Dan Knights15.   

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.

Entities:  

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

Mesh:

Substances:

Year:  2016        PMID: 27573830      PMCID: PMC5027417          DOI: 10.1073/pnas.1521835113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  40 in total

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2.  Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB.

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Review 3.  The causes of intestinal dysbiosis: a review.

Authors:  Jason A Hawrelak; Stephen P Myers
Journal:  Altern Med Rev       Date:  2004-06

4.  High-fat diet determines the composition of the murine gut microbiome independently of obesity.

Authors:  Marie A Hildebrandt; Christian Hoffmann; Scott A Sherrill-Mix; Sue A Keilbaugh; Micah Hamady; Ying-Yu Chen; Rob Knight; Rexford S Ahima; Frederic Bushman; Gary D Wu
Journal:  Gastroenterology       Date:  2009-08-23       Impact factor: 22.682

5.  Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome.

Authors:  Peter J Turnbaugh; Fredrik Bäckhed; Lucinda Fulton; Jeffrey I Gordon
Journal:  Cell Host Microbe       Date:  2008-04-17       Impact factor: 21.023

6.  Linking long-term dietary patterns with gut microbial enterotypes.

Authors:  Gary D Wu; Jun Chen; Christian Hoffmann; Kyle Bittinger; Ying-Yu Chen; Sue A Keilbaugh; Meenakshi Bewtra; Dan Knights; William A Walters; Rob Knight; Rohini Sinha; Erin Gilroy; Kernika Gupta; Robert Baldassano; Lisa Nessel; Hongzhe Li; Frederic D Bushman; James D Lewis
Journal:  Science       Date:  2011-09-01       Impact factor: 47.728

7.  Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes.

Authors:  Christopher T Brown; Austin G Davis-Richardson; Adriana Giongo; Kelsey A Gano; David B Crabb; Nabanita Mukherjee; George Casella; Jennifer C Drew; Jorma Ilonen; Mikael Knip; Heikki Hyöty; Riitta Veijola; Tuula Simell; Olli Simell; Josef Neu; Clive H Wasserfall; Desmond Schatz; Mark A Atkinson; Eric W Triplett
Journal:  PLoS One       Date:  2011-10-17       Impact factor: 3.240

8.  Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity.

Authors:  Jorge Henao-Mejia; Eran Elinav; Chengcheng Jin; Liming Hao; Wajahat Z Mehal; Till Strowig; Christoph A Thaiss; Andrew L Kau; Stephanie C Eisenbarth; Michael J Jurczak; Joao-Paulo Camporez; Gerald I Shulman; Jeffrey I Gordon; Hal M Hoffman; Richard A Flavell
Journal:  Nature       Date:  2012-02-01       Impact factor: 49.962

9.  Gut microbiomes of Malawian twin pairs discordant for kwashiorkor.

Authors:  Michelle I Smith; Tanya Yatsunenko; Mark J Manary; Indi Trehan; Rajhab Mkakosya; Jiye Cheng; Andrew L Kau; Stephen S Rich; Patrick Concannon; Josyf C Mychaleckyj; Jie Liu; Eric Houpt; Jia V Li; Elaine Holmes; Jeremy Nicholson; Dan Knights; Luke K Ursell; Rob Knight; Jeffrey I Gordon
Journal:  Science       Date:  2013-01-30       Impact factor: 47.728

10.  Fat, fibre and cancer risk in African Americans and rural Africans.

Authors:  Stephen J D O'Keefe; Jia V Li; Leo Lahti; Junhai Ou; Franck Carbonero; Khaled Mohammed; Joram M Posma; James Kinross; Elaine Wahl; Elizabeth Ruder; Kishore Vipperla; Vasudevan Naidoo; Lungile Mtshali; Sebastian Tims; Philippe G B Puylaert; James DeLany; Alyssa Krasinskas; Ann C Benefiel; Hatem O Kaseb; Keith Newton; Jeremy K Nicholson; Willem M de Vos; H Rex Gaskins; Erwin G Zoetendal
Journal:  Nat Commun       Date:  2015-04-28       Impact factor: 14.919

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  168 in total

1.  Diet Versus Phylogeny: a Comparison of Gut Microbiota in Captive Colobine Monkey Species.

Authors:  Vanessa L Hale; Chia L Tan; Kefeng Niu; Yeqin Yang; Rob Knight; Qikun Zhang; Duoying Cui; Katherine R Amato
Journal:  Microb Ecol       Date:  2017-07-22       Impact factor: 4.552

2.  Improving the standards for gut microbiome analysis of fecal samples: insights from the field biology of Japanese macaques on Yakushima Island.

Authors:  Takashi Hayakawa; Akiko Sawada; Akifumi S Tanabe; Shinji Fukuda; Takushi Kishida; Yosuke Kurihara; Kei Matsushima; Jie Liu; Etienne-Francois Akomo-Okoue; Waleska Gravena; Makoto Kashima; Mariko Suzuki; Kohmei Kadowaki; Takafumi Suzumura; Eiji Inoue; Hideki Sugiura; Goro Hanya; Kiyokazu Agata
Journal:  Primates       Date:  2018-06-25       Impact factor: 2.163

Review 3.  The gut microbiome as a driver of individual variation in cognition and functional behaviour.

Authors:  Gabrielle L Davidson; Amy C Cooke; Crystal N Johnson; John L Quinn
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2018-09-26       Impact factor: 6.237

Review 4.  Primate microbiomes over time: Longitudinal answers to standing questions in microbiome research.

Authors:  Johannes R Björk; Mauna Dasari; Laura Grieneisen; Elizabeth A Archie
Journal:  Am J Primatol       Date:  2019-04-02       Impact factor: 2.371

5.  Establishment of a Macaca fascicularis gut microbiome gene catalog and comparison with the human, pig, and mouse gut microbiomes.

Authors:  Xiaoping Li; Suisha Liang; Zhongkui Xia; Jing Qu; Huan Liu; Chuan Liu; Huanming Yang; Jian Wang; Lise Madsen; Yong Hou; Junhua Li; Huijue Jia; Karsten Kristiansen; Liang Xiao
Journal:  Gigascience       Date:  2018-09-01       Impact factor: 6.524

Review 6.  A review of research in primate sanctuaries.

Authors:  Stephen R Ross; Jesse G Leinwand
Journal:  Biol Lett       Date:  2020-04-01       Impact factor: 3.703

7.  Differences in the gut microbiota between Cercopithecinae and Colobinae in captivity.

Authors:  Zongjin Huan; Yongfang Yao; Jianqiu Yu; Hongwei Chen; Meirong Li; Chaojun Yang; Bo Zhao; Qingyong Ni; Mingwang Zhang; Meng Xie; Huailiang Xu
Journal:  J Microbiol       Date:  2020-03-28       Impact factor: 3.422

Review 8.  Microbial control of host gene regulation and the evolution of host-microbiome interactions in primates.

Authors:  Laura Grieneisen; Amanda L Muehlbauer; Ran Blekhman
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-08-10       Impact factor: 6.237

9.  Rates of gut microbiome divergence in mammals.

Authors:  Alex H Nishida; Howard Ochman
Journal:  Mol Ecol       Date:  2018-01-31       Impact factor: 6.185

10.  Hierarchical social networks shape gut microbial composition in wild Verreaux's sifaka.

Authors:  Amanda C Perofsky; Rebecca J Lewis; Laura A Abondano; Anthony Di Fiore; Lauren Ancel Meyers
Journal:  Proc Biol Sci       Date:  2017-12-06       Impact factor: 5.349

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