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Title: Gut microbiota and their putative metabolic functions in fragmented Bengal tiger population of Nepal

Abstract

Bengal tigers (Panthera tigris tigris) serve a pivotal role as an apex predator in forest ecosystems. To increase our knowledge on factors impacting the viability and health of this endangered species, we studied the gut microbiota in 32 individual Bengal tigers from three geographically separated areas (Chitwan National Park (CNP), Bardia National Park (BNP) and Suklaphanta Wildlife Reserve (SWR)) in Nepal, using noninvasive genetic sampling methods. Gut microbiota influence the immune system, impact various physiological functions, and modulates metabolic reactions, that ultimately impact the host health, behavior and development. Across the tiger populations in Nepal, we found significant differences in the composition of microbial communities based on their geographic locations. Specifically, we detected significant differences between CNP and the other two protected areas (CNP vs BNP: pseudo t = 1.944, P = 0.006; CNP vs SWR: pseudo t = 1.9942, P = 0.0071), but no differences between BNP and SWR. This mirrors what has been found for tiger gene flow in the same populations, suggesting gut microbiota composition and host gene flow may be linked. Furthermore, predictive metagenome functional content analysis (PICRUSt) revealed a higher functional enrichment and diversity for significant gut microbiota in the Chitwan tiger population and themore » lowest enrichment and diversity in Suklaphanta. The CNP tiger population contained higher proportions of microbiota that are associated with predicted functions relevant for metabolism of amino acid, lipid, xenobiotics biodegradation, terpenoides and polyketides than the SWR population. We conclude the tiger population structure, gut microbiota profile and associated functional metabolic categories are correlated, with geographically most separated CNP and SWR tiger population having the most distinct and different host genotype and microbiota profiles. Our work dramatically expands the understanding of tiger microbiota in wild populations and provides a valuable case study on how to investigate genetic diversity at different hierarchical levels, including hosts as well as their microbial communities.« less

Authors:
ORCiD logo [1];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [2];  [3];  [3];  [4];  [5];  [5];  [6];  [6];  [7];  [8];  [9];  [10] more »; ORCiD logo [11];  [2] « less
  1. Center for Molecular Dynamics Nepal, Kathmandu, (Nepal); Griffith Univ., Queensland (Australia). School of Environment
  2. Center for Molecular Dynamics Nepal, Kathmandu, (Nepal)
  3. US Agency for International Development, Kathmandu, (Nepal). Environment Team
  4. Univ. of Idaho, Moscow, ID (United States). Dept. of Fish and Wildlife Sciences
  5. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States). Dept. of Fish and Wildlife Conservation
  6. Los Alamos National Lab. (LANL), Los Alamos, NM (United States). Applied Genomics
  7. Univ. of the Sunshine Coast, Queensland (Australia). School of Science and Education
  8. Griffith Univ., Queensland (Australia). School of Environment
  9. American Museum of Natural History (AMNH), New York, NY (United States). Slacker Inst. for Comparative Genomics; City Univ. of New York (CUNY), NY (United States). Hunter College. Bioinformatics and Computational Genomics Lab.
  10. City Univ. of New York (CUNY), NY (United States). Dept. of Biology; Leiden Univ. (Netherlands). Inst. of Environmental Sciences
  11. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Veterinary Population Medicine
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1627887
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 14; Journal Issue: 8; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Science & Technology - Other Topics

Citation Formats

Karmacharya, Dibesh, Manandhar, Prajwol, Manandhar, Sulochana, Sherchan, Adarsh M., Sharma, Ajay N., Joshi, Jyoti, Bista, Manisha, Bajracharya, Shailendra, Awasthi, Nagendra P., Sharma, Netra, Llewellyn, Bronwyn, Waits, Lisette P., Thapa, Kanchan, Kelly, Marcella J., Vuyisich, Momchilo, Starkenburg, Shawn R., Hero, Jean-Marc, Hughes, Jane, Wultsch, Claudia, Bertola, Laura, Fountain-Jones, Nicholas M., and Sinha, Amit K.. Gut microbiota and their putative metabolic functions in fragmented Bengal tiger population of Nepal. United States: N. p., 2019. Web. https://doi.org/10.1371/journal.pone.0221868.
Karmacharya, Dibesh, Manandhar, Prajwol, Manandhar, Sulochana, Sherchan, Adarsh M., Sharma, Ajay N., Joshi, Jyoti, Bista, Manisha, Bajracharya, Shailendra, Awasthi, Nagendra P., Sharma, Netra, Llewellyn, Bronwyn, Waits, Lisette P., Thapa, Kanchan, Kelly, Marcella J., Vuyisich, Momchilo, Starkenburg, Shawn R., Hero, Jean-Marc, Hughes, Jane, Wultsch, Claudia, Bertola, Laura, Fountain-Jones, Nicholas M., & Sinha, Amit K.. Gut microbiota and their putative metabolic functions in fragmented Bengal tiger population of Nepal. United States. https://doi.org/10.1371/journal.pone.0221868
Karmacharya, Dibesh, Manandhar, Prajwol, Manandhar, Sulochana, Sherchan, Adarsh M., Sharma, Ajay N., Joshi, Jyoti, Bista, Manisha, Bajracharya, Shailendra, Awasthi, Nagendra P., Sharma, Netra, Llewellyn, Bronwyn, Waits, Lisette P., Thapa, Kanchan, Kelly, Marcella J., Vuyisich, Momchilo, Starkenburg, Shawn R., Hero, Jean-Marc, Hughes, Jane, Wultsch, Claudia, Bertola, Laura, Fountain-Jones, Nicholas M., and Sinha, Amit K.. Thu . "Gut microbiota and their putative metabolic functions in fragmented Bengal tiger population of Nepal". United States. https://doi.org/10.1371/journal.pone.0221868. https://www.osti.gov/servlets/purl/1627887.
@article{osti_1627887,
title = {Gut microbiota and their putative metabolic functions in fragmented Bengal tiger population of Nepal},
author = {Karmacharya, Dibesh and Manandhar, Prajwol and Manandhar, Sulochana and Sherchan, Adarsh M. and Sharma, Ajay N. and Joshi, Jyoti and Bista, Manisha and Bajracharya, Shailendra and Awasthi, Nagendra P. and Sharma, Netra and Llewellyn, Bronwyn and Waits, Lisette P. and Thapa, Kanchan and Kelly, Marcella J. and Vuyisich, Momchilo and Starkenburg, Shawn R. and Hero, Jean-Marc and Hughes, Jane and Wultsch, Claudia and Bertola, Laura and Fountain-Jones, Nicholas M. and Sinha, Amit K.},
abstractNote = {Bengal tigers (Panthera tigris tigris) serve a pivotal role as an apex predator in forest ecosystems. To increase our knowledge on factors impacting the viability and health of this endangered species, we studied the gut microbiota in 32 individual Bengal tigers from three geographically separated areas (Chitwan National Park (CNP), Bardia National Park (BNP) and Suklaphanta Wildlife Reserve (SWR)) in Nepal, using noninvasive genetic sampling methods. Gut microbiota influence the immune system, impact various physiological functions, and modulates metabolic reactions, that ultimately impact the host health, behavior and development. Across the tiger populations in Nepal, we found significant differences in the composition of microbial communities based on their geographic locations. Specifically, we detected significant differences between CNP and the other two protected areas (CNP vs BNP: pseudo t = 1.944, P = 0.006; CNP vs SWR: pseudo t = 1.9942, P = 0.0071), but no differences between BNP and SWR. This mirrors what has been found for tiger gene flow in the same populations, suggesting gut microbiota composition and host gene flow may be linked. Furthermore, predictive metagenome functional content analysis (PICRUSt) revealed a higher functional enrichment and diversity for significant gut microbiota in the Chitwan tiger population and the lowest enrichment and diversity in Suklaphanta. The CNP tiger population contained higher proportions of microbiota that are associated with predicted functions relevant for metabolism of amino acid, lipid, xenobiotics biodegradation, terpenoides and polyketides than the SWR population. We conclude the tiger population structure, gut microbiota profile and associated functional metabolic categories are correlated, with geographically most separated CNP and SWR tiger population having the most distinct and different host genotype and microbiota profiles. Our work dramatically expands the understanding of tiger microbiota in wild populations and provides a valuable case study on how to investigate genetic diversity at different hierarchical levels, including hosts as well as their microbial communities.},
doi = {10.1371/journal.pone.0221868},
journal = {PLoS ONE},
number = 8,
volume = 14,
place = {United States},
year = {2019},
month = {8}
}

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