Abstract

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. IMPORTANCE 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.

Highlights

  • 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

  • We use as a model the captive Komodo dragon (Varanus komodoensis), applying 16S rRNA amplicon sequencing to characterize the oral, fecal, skin, and environment-associated microbiomes to answer two main questions: first, is the extent of host-environment microbiome sharing observed for captive Komodo dragons typical of that observed among other vertebrates living in closed environments, and second, is the host-environment microbiome sharing observed among captive Komodo dragons characteristically different from that observed among wild vertebrates? To answer these questions, we explored whether host-environment microbiome sharing in captive Komodo dragons was similar to the pattern observed for humans and pets living in homes and dissimilar to the pattern observed among wild amphibians living in open ecosystems

  • This study represents the first description of the captive Komodo dragon skin and fecal microbial communities, filling an important knowledge gap, as previous studies have focused on the Komodo dragon salivary microbiome [11, 16]

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Summary

Introduction

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. 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. 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. The average number of bacterial species cultivated from the mouths of wild Komodo dragons was reported to be 46% higher than the number isolated from captive dragons, this study leveraged culture-dependent methods, rather than culture-independent, sequencing-based protocols [11]

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