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Title: The Oral and Skin Microbiomes of Captive Komodo Dragons Are Significantly Shared with Their Habitat

Abstract

Animals, including humans, have evolved in the context of exposure to a variety of microbial organisms present in the environment. Only recently have humans, and some animals, begun to spend a significant amount of time in enclosed artificial environments, rather than in the more natural spaces in which most of evolution took place. The consequences of this radical change in lifestyle likely extend to the microbes residing in and on our bodies and may have important implications for health and disease. A full characterization of host-microbe sharing in both closed and open environments will provide crucial information that may enable the improvement of health in humans and in captive animals, both of which experience a greater incidence of disease (including chronic illness) than counterparts living under more ecologically natural conditions. Examining the way in which animals, including those in captivity, interact with their environment is extremely important for studying ecological processes and developing sophisticated animal husbandry. Here we use the Komodo dragon (Varanus komodoensis) to quantify the degree of sharing of salivary, skin, and fecal microbiota with their environment in captivity. Both species richness and microbial community composition of most surfaces in the Komodo dragon’s environment are similar to themore » Komodo dragon’s salivary and skin microbiota but less similar to the stool-associated microbiota. We additionally compared host-environment microbiome sharing between captive Komodo dragons and their enclosures, humans and pets and their homes, and wild amphibians and their environments. We observed similar host-environment microbiome sharing patterns among humans and their pets and Komodo dragons, with high levels of human/pet- and Komodo dragon-associated microbes on home and enclosure surfaces. In contrast, only small amounts of amphibian-associated microbes were detected in the animals’ environments. We suggest that the degree of sharing between the Komodo dragon microbiota and its enclosure surfaces has important implications for animal health. These animals evolved in the context of constant exposure to a complex environmental microbiota, which likely shaped their physiological development; in captivity, these animals will not receive significant exposure to microbes not already in their enclosure, with unknown consequences for their health. Animals, including humans, have evolved in the context of exposure to a variety of microbial organisms present in the environment. Only recently have humans, and some animals, begun to spend a significant amount of time in enclosed artificial environments, rather than in the more natural spaces in which most of evolution took place. The consequences of this radical change in lifestyle likely extend to the microbes residing in and on our bodies and may have important implications for health and disease. A full characterization of host-microbe sharing in both closed and open environments will provide crucial information that may enable the improvement of health in humans and in captive animals, both of which experience a greater incidence of disease (including chronic illness) than counterparts living under more ecologically natural conditions.« less

Authors:
 [1];  [2]; ORCiD logo [3];  [4];  [1];  [5];  [6];  [7];  [8];  [9];  [10];  [11];  [12];
  1. Univ. of Colorado, Boulder, CO (United States). BioFrontiers Institute
  2. Univ. of Colorado, Boulder, CO (United States), Dept. of Computer Science
  3. Univ. of Colorado, Boulder, CO (United States). BioFrontiers Institute; Univ. of Colorado, Boulder, CO (United States). Dept. of Ecology and Evolutionary Biology
  4. Univ. of Colorado, Boulder, CO (United States). Dept. of Ecology and Evolutionary Biology
  5. Univ. of Chicago, IL (United States). Graduate Program in Biophysical Sciences
  6. Univ. of Colorado, Boulder, CO (United States). BioFrontiers Institute
  7. Department of Herpetology, Bronx Zoo/WCS, Bronx, New York, USA
  8. Denver Zoological Foundation, Denver, CO (United States)
  9. Zoo Atlanta, Atlanta, GA (United States); Georgia Inst. of Technology, Atlanta, GA (United States). School of Biology
  10. Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, Colorado, USA
  11. Biosciences Department, Institute for Genomics and Systems Biology, Argonne National Laboratory, Argonne, Illinois, USA; Departments of Ecology and Evolution and Surgery, University of Chicago, Chicago, Illinois, USA
  12. BioFrontiers Institute, University of Colorado Boulder, Boulder, Colorado, USA; Departments of Chemistry and Biochemistry and Computer Science, University of Colorado Boulder, Boulder, Colorado, USA
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1626166
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
mSystems
Additional Journal Information:
Journal Volume: 1; Journal Issue: 4; Journal ID: ISSN 2379-5077
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Microbiology; Komodo dragon; SourceTracker; built environment; human microbiome; microbiome

Citation Formats

Hyde, Embriette R., Navas-Molina, Jose A., Song, Se Jin, Kueneman, Jordan G., Ackermann, Gail, Cardona, Cesar, Humphrey, Gregory, Boyer, Don, Weaver, Tom, Mendelson, Joseph R., McKenzie, Valerie J., Gilbert, Jack A., Knight, Rob, and Shade, Ashley. The Oral and Skin Microbiomes of Captive Komodo Dragons Are Significantly Shared with Their Habitat. United States: N. p., 2016. Web. https://doi.org/10.1128/msystems.00046-16.
Hyde, Embriette R., Navas-Molina, Jose A., Song, Se Jin, Kueneman, Jordan G., Ackermann, Gail, Cardona, Cesar, Humphrey, Gregory, Boyer, Don, Weaver, Tom, Mendelson, Joseph R., McKenzie, Valerie J., Gilbert, Jack A., Knight, Rob, & Shade, Ashley. The Oral and Skin Microbiomes of Captive Komodo Dragons Are Significantly Shared with Their Habitat. United States. https://doi.org/10.1128/msystems.00046-16
Hyde, Embriette R., Navas-Molina, Jose A., Song, Se Jin, Kueneman, Jordan G., Ackermann, Gail, Cardona, Cesar, Humphrey, Gregory, Boyer, Don, Weaver, Tom, Mendelson, Joseph R., McKenzie, Valerie J., Gilbert, Jack A., Knight, Rob, and Shade, Ashley. Tue . "The Oral and Skin Microbiomes of Captive Komodo Dragons Are Significantly Shared with Their Habitat". United States. https://doi.org/10.1128/msystems.00046-16. https://www.osti.gov/servlets/purl/1626166.
@article{osti_1626166,
title = {The Oral and Skin Microbiomes of Captive Komodo Dragons Are Significantly Shared with Their Habitat},
author = {Hyde, Embriette R. and Navas-Molina, Jose A. and Song, Se Jin and Kueneman, Jordan G. and Ackermann, Gail and Cardona, Cesar and Humphrey, Gregory and Boyer, Don and Weaver, Tom and Mendelson, Joseph R. and McKenzie, Valerie J. and Gilbert, Jack A. and Knight, Rob and Shade, Ashley},
abstractNote = {Animals, including humans, have evolved in the context of exposure to a variety of microbial organisms present in the environment. Only recently have humans, and some animals, begun to spend a significant amount of time in enclosed artificial environments, rather than in the more natural spaces in which most of evolution took place. The consequences of this radical change in lifestyle likely extend to the microbes residing in and on our bodies and may have important implications for health and disease. A full characterization of host-microbe sharing in both closed and open environments will provide crucial information that may enable the improvement of health in humans and in captive animals, both of which experience a greater incidence of disease (including chronic illness) than counterparts living under more ecologically natural conditions. Examining the way in which animals, including those in captivity, interact with their environment is extremely important for studying ecological processes and developing sophisticated animal husbandry. Here we use the Komodo dragon (Varanus komodoensis) to quantify the degree of sharing of salivary, skin, and fecal microbiota with their environment in captivity. Both species richness and microbial community composition of most surfaces in the Komodo dragon’s environment are similar to the Komodo dragon’s salivary and skin microbiota but less similar to the stool-associated microbiota. We additionally compared host-environment microbiome sharing between captive Komodo dragons and their enclosures, humans and pets and their homes, and wild amphibians and their environments. We observed similar host-environment microbiome sharing patterns among humans and their pets and Komodo dragons, with high levels of human/pet- and Komodo dragon-associated microbes on home and enclosure surfaces. In contrast, only small amounts of amphibian-associated microbes were detected in the animals’ environments. We suggest that the degree of sharing between the Komodo dragon microbiota and its enclosure surfaces has important implications for animal health. These animals evolved in the context of constant exposure to a complex environmental microbiota, which likely shaped their physiological development; in captivity, these animals will not receive significant exposure to microbes not already in their enclosure, with unknown consequences for their health. Animals, including humans, have evolved in the context of exposure to a variety of microbial organisms present in the environment. Only recently have humans, and some animals, begun to spend a significant amount of time in enclosed artificial environments, rather than in the more natural spaces in which most of evolution took place. The consequences of this radical change in lifestyle likely extend to the microbes residing in and on our bodies and may have important implications for health and disease. A full characterization of host-microbe sharing in both closed and open environments will provide crucial information that may enable the improvement of health in humans and in captive animals, both of which experience a greater incidence of disease (including chronic illness) than counterparts living under more ecologically natural conditions.},
doi = {10.1128/msystems.00046-16},
journal = {mSystems},
number = 4,
volume = 1,
place = {United States},
year = {2016},
month = {8}
}

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Works referenced in this record:

The bacterial microbiota in the ceca of Capercaillie (Tetrao urogallus) differs between wild and captive birds
journal, November 2011

  • Wienemann, Tobias; Schmitt-Wagner, Dirk; Meuser, Katja
  • Systematic and Applied Microbiology, Vol. 34, Issue 7
  • DOI: 10.1016/j.syapm.2011.06.003

ANAEROBIC AND AEROBIC BACTERIOLOGY OF THE SALIVA AND GINGIVA FROM 16 CAPTIVE KOMODO DRAGONS ( VARANUS KOMODOENSIS ): NEW IMPLICATIONS FOR THE “BACTERIA AS VENOM” MODEL
journal, June 2013

  • Goldstein, Ellie J. C.; Tyrrell, Kerin L.; Citron, Diane M.
  • Journal of Zoo and Wildlife Medicine, Vol. 44, Issue 2
  • DOI: 10.1638/2012-0022R.1

Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity
journal, April 2007

  • Uenishi, Gentaro; Fujita, Shiho; Ohashi, Gaku
  • American Journal of Primatology, Vol. 69, Issue 4
  • DOI: 10.1002/ajp.20351

Transfer of Fermentative Microbes Between Generations in a Herbivorous Lizard
journal, April 1982


Longitudinal analysis of microbial interaction between humans and the indoor environment
journal, August 2014


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

Family size, infection and atopy: the first decade of the 'hygiene hypothesis'
journal, August 2000


Aerobic Salivary Bacteria in wild and Captive Komodo Dragons
journal, July 2002

  • Montgomery, Joel M.; Gillespie, Don; Sastrawan, Putra
  • Journal of Wildlife Diseases, Vol. 38, Issue 3
  • DOI: 10.7589/0090-3558-38.3.545

In Search of a Germ Theory Equivalent for Chronic Disease
journal, May 2012


Euphorbia plant latex is inhabited by diverse microbial communities
journal, December 2015

  • Gunawardana, Manjula; Hyde, Embriette R.; Lahmeyer, Sean
  • American Journal of Botany, Vol. 102, Issue 12
  • DOI: 10.3732/ajb.1500223

Microbes, herbivory and the evolution of social behavior
journal, January 1984


The effect of captivity on the cutaneous bacterial community of the critically endangered Panamanian golden frog (Atelopus zeteki)
journal, August 2014


Behavioral acquisition of the hindgut fermentation system by hatchling Iguana iguana
journal, March 1984

  • Troyer, Katherine
  • Behavioral Ecology and Sociobiology, Vol. 14, Issue 3
  • DOI: 10.1007/BF00299618

Animals in a bacterial world, a new imperative for the life sciences
journal, February 2013

  • McFall-Ngai, Margaret; Hadfield, Michael G.; Bosch, Thomas C. G.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
  • DOI: 10.1073/pnas.1218525110

The amphibian skin-associated microbiome across species, space and life history stages
journal, October 2013

  • Kueneman, Jordan G.; Parfrey, Laura Wegener; Woodhams, Douglas C.
  • Molecular Ecology, Vol. 23, Issue 6
  • DOI: 10.1111/mec.12510

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

Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus)
journal, December 2013

  • Loudon, Andrew H.; Woodhams, Douglas C.; Parfrey, Laura Wegener
  • The ISME Journal, Vol. 8, Issue 4
  • DOI: 10.1038/ismej.2013.200

The microbiome of uncontacted Amerindians
journal, April 2015

  • Clemente, Jose C.; Pehrsson, Erica C.; Blaser, Martin J.
  • Science Advances, Vol. 1, Issue 3
  • DOI: 10.1126/sciadv.1500183

Survey and comparison of major intestinal flora in captive and wild ring-tailed lemur (Lemur catta) populations
journal, February 2008

  • Villers, Lynne M.; Jang, Spencer S.; Lent, Cheryl L.
  • American Journal of Primatology, Vol. 70, Issue 2
  • DOI: 10.1002/ajp.20482

Changes in the Intestinal Microbiota of Wild Atlantic cod Gadus morhua L. Upon Captive Rearing
journal, April 2010

  • Dhanasiri, Anusha K. S.; Brunvold, Laila; Brinchmann, Monica F.
  • Microbial Ecology, Vol. 61, Issue 1
  • DOI: 10.1007/s00248-010-9673-y

Comparison of the Cecal Microbiota of Domestic and Wild Turkeys
journal, January 2008


Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale
journal, June 2009

  • Lauber, C. L.; Hamady, M.; Knight, R.
  • Applied and Environmental Microbiology, Vol. 75, Issue 15
  • DOI: 10.1128/AEM.00335-09

A RETROSPECTIVE STUDY OF END-STAGE RENAL DISEASE IN CAPTIVE POLAR BEARS ( URSUS MARITIMUS )
journal, March 2014

  • LaDouceur, Elise E. B.; Garner, Michael M.; Davis, Barbara
  • Journal of Zoo and Wildlife Medicine, Vol. 45, Issue 1
  • DOI: 10.1638/2013-0071R.1

Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences
journal, January 2014

  • Rideout, Jai Ram; He, Yan; Navas-Molina, Jose A.
  • PeerJ, Vol. 2
  • DOI: 10.7717/peerj.545

Wild-caught rodents retain a majority of their natural gut microbiota upon entrance into captivity: Effect of captivity on rodent gut microbiota
journal, November 2013

  • Kohl, Kevin D.; Dearing, M. Denise
  • Environmental Microbiology Reports, Vol. 6, Issue 2
  • DOI: 10.1111/1758-2229.12118

INTESTINAL AND CLOACAL STRICTURES IN FREE-RANGING AND AQUARIUM-MAINTAINED GREEN SEA TURTLES ( CHELONIA MYDAS )
journal, June 2013

  • Erlacher-Reid, Claire D.; Norton, Terry M.; Harms, Craig A.
  • Journal of Zoo and Wildlife Medicine, Vol. 44, Issue 2
  • DOI: 10.1638/2012-0071R.1

The diversity and biogeography of soil bacterial communities
journal, January 2006

  • Fierer, N.; Jackson, R. B.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 3
  • DOI: 10.1073/pnas.0507535103

Molecular characterization of the cloacal microbiota of wild and captive parrots
journal, December 2010

  • Xenoulis, Panagiotis G.; Gray, Patricia L.; Brightsmith, Donald
  • Veterinary Microbiology, Vol. 146, Issue 3-4
  • DOI: 10.1016/j.vetmic.2010.05.024

Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms
journal, March 2012

  • Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A.
  • The ISME Journal, Vol. 6, Issue 8
  • DOI: 10.1038/ismej.2012.8

EMPeror: a tool for visualizing high-throughput microbial community data
journal, November 2013

  • Vázquez-Baeza, Yoshiki; Pirrung, Meg; Gonzalez, Antonio
  • GigaScience, Vol. 2, Issue 1
  • DOI: 10.1186/2047-217X-2-16

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


Bayesian community-wide culture-independent microbial source tracking
journal, July 2011

  • Knights, Dan; Kuczynski, Justin; Charlson, Emily S.
  • Nature Methods, Vol. 8, Issue 9
  • DOI: 10.1038/nmeth.1650

Search and clustering orders of magnitude faster than BLAST
journal, August 2010


Our interface with the built environment: immunity and the indoor microbiota
journal, March 2015


Amphibian skin may select for rare environmental microbes
journal, May 2014

  • Walke, Jenifer B.; Becker, Matthew H.; Loftus, Stephen C.
  • The ISME Journal, Vol. 8, Issue 11
  • DOI: 10.1038/ismej.2014.77

UniFrac: a New Phylogenetic Method for Comparing Microbial Communities
journal, December 2005


Cohabiting family members share microbiota with one another and with their dogs
journal, April 2013

  • Song, Se Jin; Lauber, Christian; Costello, Elizabeth K.
  • eLife, Vol. 2
  • DOI: 10.7554/eLife.00458

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 Gut Microbiome in Autism: Study-Site Effects and Longitudinal Analysis of Behavior Change
journal, April 2021


    Works referencing / citing this record:

    Amphibian chytridiomycosis outbreak dynamics are linked with host skin bacterial community structure
    journal, February 2018


    Evaluating the impact of domestication and captivity on the horse gut microbiome
    journal, November 2017


    Habitat environments impacted the gut microbiome of long-distance migratory swan geese but central species conserved
    journal, September 2018


    Metagenomic analysis of dental calculus in ancient Egyptian baboons
    journal, December 2019


    The Effects of Captivity on the Mammalian Gut Microbiome
    journal, August 2017

    • McKenzie, Valerie J.; Song, Se Jin; Delsuc, Frédéric
    • Integrative and Comparative Biology, Vol. 57, Issue 4
    • DOI: 10.1093/icb/icx090

    Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices
    journal, January 2019

    • Trevelline, Brian K.; Fontaine, Samantha S.; Hartup, Barry K.
    • Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1895
    • DOI: 10.1098/rspb.2018.2448

    The Skin Microbiome of Cohabiting Couples
    journal, July 2017


    Environmental Sources of Bacteria Differentially Influence Host-Associated Microbial Dynamics
    journal, May 2018


    Highly Reproducible 16S Sequencing Facilitates Measurement of Host Genetic Influences on the Stickleback Gut Microbiome
    journal, August 2019


    Engineering the microbiome for animal health and conservation
    journal, February 2019

    • Jin Song, Se; Woodhams, Douglas C.; Martino, Cameron
    • Experimental Biology and Medicine, Vol. 244, Issue 6
    • DOI: 10.1177/1535370219830075

    Skin and gut microbiomes of a wild mammal respond to different environmental cues
    journal, November 2018


    The skin microbiome of vertebrates
    journal, May 2019


    Looking like the locals - gut microbiome changes post-release in an endangered species
    journal, October 2019


    Bacterial Communities in Boreal Forest Mushrooms Are Shaped Both by Soil Parameters and Host Identity
    journal, May 2017


    One Health Relationships Between Human, Animal, and Environmental Microbiomes: A Mini-Review
    journal, August 2018


    Evaluating the impact of domestication and captivity on the horse gut microbiome.
    text, January 2017

    • Metcalf, Jessica L.; Song, Se Jin; Morton, James T.
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.18005