Associations Between Nutrition, Gut Microbiome, and Health in A Novel Nonhuman Primate Model

Jonathan B. Clayton; Gabriel A. Al-Ghalith; Ha Thang Long; Bui Van Tuan; Francis Cabana; Hu Huang; Pajau Vangay; Tonya Ward; Vo Van Minh; Nguyen Ai Tam; Nguyen Tat Dat; Dominic A. Travis; Michael P. Murtaugh; Herbert Covert; Kenneth E. Glander; Tilo Nadler; Barbara Toddes; John C.M. Sha; Randy Singer; Dan Knights; Timothy J. Johnson

doi:10.1038/s41598-018-29277-x

Associations Between Nutrition, Gut Microbiome, and Health in A Novel Nonhuman Primate Model

Jonathan B. Clayton, Gabriel A. Al-Ghalith, Ha Thang Long, Bui Van Tuan, Francis Cabana, Hu Huang, Pajau Vangay, Tonya Ward, Vo Van Minh, Nguyen Ai Tam, Nguyen Tat Dat, Dominic A. Travis, Michael P. Murtaugh, Herbert Covert, Kenneth E. Glander, Tilo Nadler, Barbara Toddes, John C.M. Sha, Randy Singer, Dan KnightsTimothy J. Johnson

Research output: Contribution to journal › Article › peer-review

37 Scopus citations

Abstract

Red-shanked doucs (Pygathrix nemaeus) are endangered, foregut-fermenting colobine primates which are difficult to maintain in captivity. There are critical gaps in our understanding of their natural lifestyle, including dietary habits such as consumption of leaves, unripe fruit, flowers, seeds, and other plant parts. There is also a lack of understanding of enteric adaptations, including their unique microflora. To address these knowledge gaps, we used the douc as a model to study relationships between gastrointestinal microbial community structure and lifestyle. We analyzed published fecal samples as well as detailed dietary history from doucs with four distinct lifestyles (wild, semi-wild, semi-captive, and captive) and determined gastrointestinal bacterial microbiome composition using 16S rRNA sequencing. A clear gradient of microbiome composition was revealed along an axis of natural lifestyle disruption, including significant associations with diet, biodiversity, and microbial function. We also identified potential microbial biomarkers of douc dysbiosis, including Bacteroides and Prevotella, which may be related to health. Our results suggest a gradient-like shift in captivity causes an attendant shift to severe gut dysbiosis, thereby resulting in gastrointestinal issues.

Original language	English (US)
Article number	11159
Journal	Scientific reports
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41598-018-29277-x
State	Published - Dec 1 2018

Bibliographical note

Funding Information:
We thank the Endangered Primate Rescue Center, Singapore Zoo, and Philadelphia Zoo for providing fecal samples from semi-wild, semi-captive, and captive red-shanked doucs; 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 Da Nang 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 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) awarded to JBC.

Publisher Copyright:
© 2018, The Author(s).

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10.1038/s41598-018-29277-x

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6057944

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Clayton, J. B., Al-Ghalith, G. A., Long, H. T., Tuan, B. V., Cabana, F., Huang, H., Vangay, P., Ward, T., Minh, V. V., Tam, N. A., Dat, N. T., Travis, D. A., Murtaugh, M. P., Covert, H., Glander, K. E., Nadler, T., Toddes, B., Sha, J. C. M., Singer, R., ... Johnson, T. J. (2018). Associations Between Nutrition, Gut Microbiome, and Health in A Novel Nonhuman Primate Model. Scientific reports, 8(1), [11159]. https://doi.org/10.1038/s41598-018-29277-x

Clayton, JB, Al-Ghalith, GA, Long, HT, Tuan, BV, Cabana, F, Huang, H, Vangay, P, Ward, T, Minh, VV, Tam, NA, Dat, NT, Travis, DA, Murtaugh, MP, Covert, H, Glander, KE, Nadler, T, Toddes, B, Sha, JCM, Singer, R, Knights, D & Johnson, TJ 2018, 'Associations Between Nutrition, Gut Microbiome, and Health in A Novel Nonhuman Primate Model', Scientific reports, vol. 8, no. 1, 11159. https://doi.org/10.1038/s41598-018-29277-x

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title = "Associations Between Nutrition, Gut Microbiome, and Health in A Novel Nonhuman Primate Model",

abstract = "Red-shanked doucs (Pygathrix nemaeus) are endangered, foregut-fermenting colobine primates which are difficult to maintain in captivity. There are critical gaps in our understanding of their natural lifestyle, including dietary habits such as consumption of leaves, unripe fruit, flowers, seeds, and other plant parts. There is also a lack of understanding of enteric adaptations, including their unique microflora. To address these knowledge gaps, we used the douc as a model to study relationships between gastrointestinal microbial community structure and lifestyle. We analyzed published fecal samples as well as detailed dietary history from doucs with four distinct lifestyles (wild, semi-wild, semi-captive, and captive) and determined gastrointestinal bacterial microbiome composition using 16S rRNA sequencing. A clear gradient of microbiome composition was revealed along an axis of natural lifestyle disruption, including significant associations with diet, biodiversity, and microbial function. We also identified potential microbial biomarkers of douc dysbiosis, including Bacteroides and Prevotella, which may be related to health. Our results suggest a gradient-like shift in captivity causes an attendant shift to severe gut dysbiosis, thereby resulting in gastrointestinal issues.",

author = "Clayton, {Jonathan B.} and Al-Ghalith, {Gabriel A.} and Long, {Ha Thang} and Tuan, {Bui Van} and Francis Cabana and Hu Huang and Pajau Vangay and Tonya Ward and Minh, {Vo Van} and Tam, {Nguyen Ai} and Dat, {Nguyen Tat} and Travis, {Dominic A.} and Murtaugh, {Michael P.} and Herbert Covert and Glander, {Kenneth E.} and Tilo Nadler and Barbara Toddes and Sha, {John C.M.} and Randy Singer and Dan Knights and Johnson, {Timothy J.}",

note = "Funding Information: We thank the Endangered Primate Rescue Center, Singapore Zoo, and Philadelphia Zoo for providing fecal samples from semi-wild, semi-captive, and captive red-shanked doucs; 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 Da Nang 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 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) awarded to JBC. Publisher Copyright: {\textcopyright} 2018, The Author(s).",

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AU - Clayton, Jonathan B.

AU - Al-Ghalith, Gabriel A.

AU - Long, Ha Thang

AU - Tuan, Bui Van

AU - Cabana, Francis

AU - Huang, Hu

AU - Vangay, Pajau

AU - Ward, Tonya

AU - Minh, Vo Van

AU - Tam, Nguyen Ai

AU - Dat, Nguyen Tat

AU - Travis, Dominic A.

AU - Murtaugh, Michael P.

AU - Covert, Herbert

AU - Glander, Kenneth E.

AU - Nadler, Tilo

AU - Toddes, Barbara

AU - Sha, John C.M.

AU - Singer, Randy

AU - Knights, Dan

AU - Johnson, Timothy J.

N1 - Funding Information: We thank the Endangered Primate Rescue Center, Singapore Zoo, and Philadelphia Zoo for providing fecal samples from semi-wild, semi-captive, and captive red-shanked doucs; 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 Da Nang 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 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) awarded to JBC. Publisher Copyright: © 2018, The Author(s).

PY - 2018/12/1

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N2 - Red-shanked doucs (Pygathrix nemaeus) are endangered, foregut-fermenting colobine primates which are difficult to maintain in captivity. There are critical gaps in our understanding of their natural lifestyle, including dietary habits such as consumption of leaves, unripe fruit, flowers, seeds, and other plant parts. There is also a lack of understanding of enteric adaptations, including their unique microflora. To address these knowledge gaps, we used the douc as a model to study relationships between gastrointestinal microbial community structure and lifestyle. We analyzed published fecal samples as well as detailed dietary history from doucs with four distinct lifestyles (wild, semi-wild, semi-captive, and captive) and determined gastrointestinal bacterial microbiome composition using 16S rRNA sequencing. A clear gradient of microbiome composition was revealed along an axis of natural lifestyle disruption, including significant associations with diet, biodiversity, and microbial function. We also identified potential microbial biomarkers of douc dysbiosis, including Bacteroides and Prevotella, which may be related to health. Our results suggest a gradient-like shift in captivity causes an attendant shift to severe gut dysbiosis, thereby resulting in gastrointestinal issues.

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Associations Between Nutrition, Gut Microbiome, and Health in A Novel Nonhuman Primate Model

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