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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
+ Show Author Affiliations
  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. doi:10.1371/journal.pone.0221868.
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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
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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.
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@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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Works referenced in this record:

Evolution of Mammals and Their Gut Microbes
journal, June 2008

From lifetime to evolution: timescales of human gut microbiota adaptation
journal, November 2014

The gut microbiota — masters of host development and physiology
journal, February 2013

  • Sommer, Felix; Bäckhed, Fredrik
  • Nature Reviews Microbiology, Vol. 11, Issue 4
  • DOI: 10.1038/nrmicro2974

The Impact of the Gut Microbiota on Human Health: An Integrative View
journal, March 2012

Host-Gut Microbiota Metabolic Interactions
journal, June 2012

The Host Genotype Affects the Bacterial Community in the Human Gastrointestinal Tract
journal, September 2001

  • Zoetendal, Erwin G.; Akkermans, Antoon D. L.; Akkermans-van Vliet, Wilma M.
  • Microbial Ecology in Health & Disease, Vol. 13, Issue 3
  • DOI: 10.3402/mehd.v13i3.8013

Conservation and the Microbiome: Editorial
journal, March 2012

Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine
journal, February 2006

Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park
journal, July 2012

  • Degnan, P. H.; Pusey, A. E.; Lonsdorf, E. V.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 32
  • DOI: 10.1073/pnas.1110994109

Social networks predict gut microbiome composition in wild baboons
journal, March 2015

Gut Microbiome of Coexisting BaAka Pygmies and Bantu Reflects Gradients of Traditional Subsistence Patterns
journal, March 2016

Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation
journal, October 2015

  • Barelli, Claudia; Albanese, Davide; Donati, Claudio
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep14862

Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes
journal, March 2013

  • Amato, Katherine R.; Yeoman, Carl J.; Kent, Angela
  • The ISME Journal, Vol. 7, Issue 7
  • DOI: 10.1038/ismej.2013.16

Diet and Environment Shape Fecal Bacterial Microbiota Composition and Enteric Pathogen Load of Grizzly Bears
journal, December 2011

Gut microbiome composition and metabolomic profiles of wild western lowland gorillas ( Gorilla gorilla gorilla ) reflect host ecology
journal, April 2015

  • Gomez, Andres; Petrzelkova, Klara; Yeoman, Carl J.
  • Molecular Ecology, Vol. 24, Issue 10
  • DOI: 10.1111/mec.13181

Gut microbial communities of American pikas ( Ochotona princeps ): Evidence for phylosymbiosis and adaptations to novel diets
journal, June 2017

  • Kohl, Kevin D.; Varner, Johanna; Wilkening, Jennifer L.
  • Journal of Animal Ecology, Vol. 87, Issue 2
  • DOI: 10.1111/1365-2656.12692

Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography: MICROBIOME ANALYSIS AMONG BATS
journal, April 2012

Co-evolution in context: The importance of studying gut microbiomes in wild animals
journal, January 2013

The current future understanding of inflammatory bowel disease
journal, December 2002

  • Podolsky, Daniel K.
  • Best Practice & Research Clinical Gastroenterology, Vol. 16, Issue 6
  • DOI: 10.1053/bega.2002.0354

Defects in mucosal immunity leading to ulcerative colitis
journal, August 2005

The gut microbiota shapes intestinal immune responses during health and disease
journal, May 2009

  • Round, June L.; Mazmanian, Sarkis K.
  • Nature Reviews Immunology, Vol. 9, Issue 5
  • DOI: 10.1038/nri2515

Intestinal Microbiota of Dogs and Cats: a Bigger World than We Thought
journal, March 2011

  • Suchodolski, Jan S.
  • Veterinary Clinics of North America: Small Animal Practice, Vol. 41, Issue 2
  • DOI: 10.1016/j.cvsm.2010.12.006

Microbiomes, metagenomics, and primate conservation: New strategies, tools, and applications
journal, July 2016

The Fate of Wild Tigers
journal, June 2007

  • Dinerstein, Eric; Loucks, Colby; Wikramanayake, Eric
  • BioScience, Vol. 57, Issue 6
  • DOI: 10.1641/B570608

Influence of prey depletion and human disturbance on tiger occupancy in Nepal: Nepal tiger occupancy
journal, August 2012

The Long-Term Effects of Tiger Poaching on Population Viability
journal, October 1995

Landscape Analysis of Tiger Distribution and Habitat Quality in Nepal
journal, December 1998

Designing a Conservation Landscape for Tigers in Human-Dominated Environments
journal, June 2004

Assessing habitat suitability for tiger in the fragmented Terai Arc Landscape of India and Nepal
journal, March 2011

Human-Carnivore Conflict and Perspectives on Carnivore Management Worldwide
journal, December 2003

The Relation Between the Number of Species and the Number of Individuals in a Random Sample of an Animal Population
journal, May 1943

  • Fisher, R. A.; Corbet, A. Steven; Williams, C. B.
  • The Journal of Animal Ecology, Vol. 12, Issue 1
  • DOI: 10.2307/1411

Trophic position determines functional and phylogenetic recovery after disturbance within a community
journal, March 2017

  • Fountain‐Jones, Nicholas M.; Jordan, Gregory J.; Burridge, Christopher P.
  • Functional Ecology, Vol. 31, Issue 7
  • DOI: 10.1111/1365-2435.12845

Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
journal, January 1995

Transfer of Multidrug-Resistant Bacteria Between Intermingled Ecological Niches: The Interface Between Humans, Animals and the Environment
journal, January 2013

  • da Costa, Paulo; Loureiro, Luís; Matos, Augusto
  • International Journal of Environmental Research and Public Health, Vol. 10, Issue 1
  • DOI: 10.3390/ijerph10010278

Diet rapidly and reproducibly alters the human gut microbiome
journal, December 2013

  • David, Lawrence A.; Maurice, Corinne F.; Carmody, Rachel N.
  • Nature, Vol. 505, Issue 7484
  • DOI: 10.1038/nature12820

Human gut microbiome viewed across age and geography
journal, May 2012

  • Yatsunenko, Tanya; Rey, Federico E.; Manary, Mark J.
  • Nature, Vol. 486, Issue 7402
  • DOI: 10.1038/nature11053

Integrated Community Profiling Indicates Long-Term Temporal Stability of the Predominant Faecal Microbiota in Captive Cheetahs
journal, April 2015

Composition and diversity of the bacterial community in snow leopard (Uncia uncia) distal gut
journal, May 2014

First report on the bacterial diversity in the distal gut of dholes (Cuon alpinus) by using 16S rRNA gene sequences analysis
journal, September 2015

Helminth infections and gut microbiota – a feline perspective
journal, December 2016

Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals: The gut microbiota of wild and captive Antarctic seals
journal, November 2012

  • Nelson, Tiffanie M.; Rogers, Tracey L.; Carlini, Alejandro R.
  • Environmental Microbiology, Vol. 15, Issue 4
  • DOI: 10.1111/1462-2920.12022

Gene-centric metagenomics analysis of feline intestinal microbiome using 454 junior pyrosequencing
journal, March 2012

  • Tun, Hein Min; Brar, Manreetpal Singh; Khin, Nina
  • Journal of Microbiological Methods, Vol. 88, Issue 3
  • DOI: 10.1016/j.mimet.2012.01.001

Comparison of the fecal microbiota of dholes high-throughput Illumina sequencing of the V3–V4 region of the 16S rRNA gene
journal, January 2016

  • Wu, Xiaoyang; Zhang, Honghai; Chen, Jun
  • Applied Microbiology and Biotechnology, Vol. 100, Issue 8
  • DOI: 10.1007/s00253-015-7257-y

Phylogenetic analysis of 16S rRNA gene sequences reveals distal gut bacterial diversity in wild wolves (Canis lupus)
journal, March 2010

Preservation of avian blood and tissue samples for DNA analyses
journal, January 1991

  • Seutin, Gilles; White, Bradley N.; Boag, Peter T.
  • Canadian Journal of Zoology, Vol. 69, Issue 1
  • DOI: 10.1139/z91-013

Optimizing collection methods for noninvasive genetic sampling of neotropical felids: Noninvasive Genetic Sampling of Wild Felids
journal, April 2015

  • Wultsch, Claudia; Waits, Lisette P.; Hallerman, Eric M.
  • Wildlife Society Bulletin, Vol. 39, Issue 2
  • DOI: 10.1002/wsb.540

Genotyping faecal samples of Bengal tiger Panthera tigris tigris for population estimation: A pilot study
journal, October 2006

A Genetic Linkage Map of Microsatellites in the Domestic Cat (Felis catus)
journal, April 1999

  • Menotti-Raymond, Marilyn; David, Victor A.; Lyons, Leslie A.
  • Genomics, Vol. 57, Issue 1
  • DOI: 10.1006/geno.1999.5743

Fourteen new di- and tetranucleotide microsatellite loci for the critically endangered Indian tiger ( Panthera tigris tigris )
journal, November 2008

An STR Forensic Typing System for Genetic Individualization of Domestic Cat ( Felis catus ) Samples
journal, January 2005

  • Menotti-Raymond, Marilyn A.; David, Victor A.; Wachter, Leslie L.
  • Journal of Forensic Sciences, Vol. 50, Issue 5
  • DOI: 10.1520/JFS2004317

Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample
journal, June 2010

  • Caporaso, J. G.; Lauber, C. L.; Walters, W. A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1000080107

QIIME allows analysis of high-throughput community sequencing data
journal, April 2010

  • Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse
  • Nature Methods, Vol. 7, Issue 5
  • DOI: 10.1038/nmeth.f.303

Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB
journal, July 2006

  • DeSantis, T. Z.; Hugenholtz, P.; Larsen, N.
  • Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072
  • DOI: 10.1128/AEM.03006-05

Stability of operational taxonomic units: an important but neglected property for analyzing microbial diversity
journal, May 2015

PyNAST: a flexible tool for aligning sequences to a template alignment
journal, November 2009

FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010

phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data
journal, April 2013

Multivariate dispersion as a measure of beta diversity
journal, June 2006

Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences
journal, August 2013

  • Langille, Morgan G. I.; Zaneveld, Jesse; Caporaso, J. Gregory
  • Nature Biotechnology, Vol. 31, Issue 9
  • DOI: 10.1038/nbt.2676

IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

KEGG for integration and interpretation of large-scale molecular data sets
journal, November 2011

  • Kanehisa, M.; Goto, S.; Sato, Y.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr988

STAMP: statistical analysis of taxonomic and functional profiles
journal, July 2014

Generalized procrustes analysis
journal, March 1975

Landscape Analysis of Tiger Distribution and Habitat Quality in Nepal
journal, December 1998

Reconstruction of ancient microbial genomes from the human gut
journal, May 2021

Microbial Dysbiosis During Simian Immunodeficiency Virus Infection is Partially Reverted with Combination Anti-retroviral Therapy
journal, April 2020

  • Blum, Faith C.; Hardy, Britney L.; Bishop-Lilly, Kimberly A.
  • Scientific Reports, Vol. 10, Issue 1
  • DOI: 10.1038/s41598-020-63196-0

The Long-Term Effects of Tiger Poaching on Population Viability
journal, October 1995

Aging features of the migratory locust at physiological and transcriptional levels
journal, April 2021

seqs.fna
dataset, January 2019

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