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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 Laboratory (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. doi: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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