Dataset Information

Deconstructing the Bat Skin Microbiome: Influences of the Host and the Environment.

ABSTRACT: Bats are geographically widespread and play an important role in many ecosystems, but relatively little is known about the ecology of their associated microbial communities and the role microbial taxa play in bat health, development, and evolution. Moreover, few vertebrate animal skin microbiomes have been comprehensively assessed, and thus characterizing the bat skin microbiome will yield valuable insight into the variability of vertebrate skin microbiomes as a whole. The recent emergence of the skin fungal disease white-nose syndrome highlights the potentially important role bat skin microbial communities could play in bat health. Understanding the determinant of bat skin microbial communities could provide insight into important factors allowing individuals to persist with disease. We collected skin swabs from a total of 11 bat species from the eastern United States (n = 45) and Colorado (n = 119), as well as environmental samples (n = 38) from a subset of sites, and used 16S rRNA marker gene sequencing to observe bacterial communities. In addition, we conducted a literature survey to compare the skin microbiome across vertebrate groups, including the bats presented in this study. Host species, region, and site were all significant predictors of the variability across bat skin bacterial communities. Many bacterial taxa were found both on bats and in the environment. However, some bacterial taxa had consistently greater relative abundances on bat skin relative to their environments. Bats shared many of their abundant taxa with other vertebrates, but also hosted unique bacterial lineages such as the class Thermoleophilia (Actinobacteria). A strong effect of site on the bat skin microbiome indicates that the environment very strongly influences what bacteria are present on bat skin. Bat skin microbiomes are largely composed of site-specific microbiota, but there do appear to be important host-specific taxa. How this translates to differences in host-microbial interactions and bat health remains an important knowledge gap, but this work suggests that habitat variability is very important. We identify some bacterial groups that are more consistent on bats despite site differences, and these may be important ones to study in terms of their function as potential core microbiome members.

SUBMITTER: Avena CV

PROVIDER: S-EPMC5112243 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Deconstructing the Bat Skin Microbiome: Influences of the Host and the Environment.

Avena Christine V CV Parfrey Laura Wegener LW Leff Jonathan W JW Archer Holly M HM Frick Winifred F WF Langwig Kate E KE Kilpatrick A Marm AM Powers Karen E KE Foster Jeffrey T JT McKenzie Valerie J VJ

Frontiers in microbiology 20161117

Bats are geographically widespread and play an important role in many ecosystems, but relatively little is known about the ecology of their associated microbial communities and the role microbial taxa play in bat health, development, and evolution. Moreover, few vertebrate animal skin microbiomes have been comprehensively assessed, and thus characterizing the bat skin microbiome will yield valuable insight into the variability of vertebrate skin microbiomes as a whole. The recent emergence of th ...[more]

PMID: 27909426

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Project description:BackgroundA wide range of microorganisms inhabit animal skin. This microbial community (microbiome) plays an important role in host defense against pathogens and disease. Bats (Chiroptera: Mammalia) are an ecologically and evolutionarily diversified group with a relatively unexplored skin microbiome. The bat skin microbiome could play a role in disease resistance, for example, to white nose syndrome (WNS), an infection which has been devastating North American bat populations. However, fundamental knowledge of the bat skin microbiome is needed before understanding its role in health and disease resistance. Captive neotropical frugivorous bats Artibeus jamaicensis and Carollia perspicillataprovide a simple controlled system in which to characterize the factors shaping the bat microbiome. Here, we aimed to determine the relative importance of habitat and host species on the bat skin microbiome.MethodsWe performed high-throughput 16S rRNA gene sequencing of the skin microbiome of two different bat species living in captivity in two different habitats. In the first habitat, A. jamaicensis and C. perspicillata lived together, while the second habitat contained only A. jamaicensis.ResultsWe found that both habitat and host species shape the composition and diversity of the skin microbiome, with habitat having the strongest influence. Cohabitating A. jamaicensis and C. perspicillata shared more similar skin microbiomes than members of the same species (A. jamaicensis) across two habitats.DiscussionThese results suggest that in captivity, the skin microbial community is homogenised by the shared environments and individual proximities of bats living together in the same habitat, at the expense of the innate host species factors. The predominant influence of habitat suggests that environmental microorganisms or pathogens might colonize bat skin. We also propose that bat populations could differ in pathogen susceptibility depending on their immediate environment and habitat.

Project description:BackgroundThe skin microbiome serves as a first line defense against pathogens in vertebrates. In amphibians, it has the potential to protect against the chytrid fungus Batrachochytrium dendrobatis (Bd), a likely agent of amphibian declines. Alteration of the microbiome associated with unfavorable environmental changes produced by anthropogenic activities may make the host more susceptible to pathogens. Some amphibian species that were thought to be "extinct" have been rediscovered years after population declines in the late 1980s probably due to evolved Bd-resistance and are now threatened by anthropogenic land-use changes. Understanding the effects of habitat disturbance on the host skin microbiome is relevant for understanding the health of these species, along with its susceptibility to pathogens such as Bd. Here, we investigate the influence of habitat alteration on the skin bacterial communities as well as specifically the putative Bd-inhibitory bacterial communities of the montane frog Lithobates vibicarius. This species, after years of not being observed, was rediscovered in small populations inhabiting undisturbed and disturbed landscapes, and with continuous presence of Bd.ResultsWe found that cutaneous bacterial communities of tadpoles and adults differed between undisturbed and disturbed habitats. The adults from disturbed habitats exhibited greater community dispersion than those from undisturbed habitats. We observed a higher richness of putative Bd-inhibitory bacterial strains in adults from disturbed habitats than in those from undisturbed habitats, as well as a greater number of these potential protective bacteria with a high relative abundance.ConclusionsOur findings support the microbial "Anna Karenina principle", in which disturbance is hypothesized to cause greater microbial dispersion in communities, a so-called dysbiosis, which is a response of animal microbiomes to stress factors that decrease the ability of the host or its microbiome to regulate community composition. On the positive side, the high richness and relative abundance of putative Bd-inhibitory bacteria may indicate the development of a defense mechanism that enhances Bd-protection, attributed to a co-occurrence of more than 30-years of host and pathogen in these disturbed habitats. Our results provide important insight into the influence of human-modified landscapes on the skin microbiome and health implications of Bd-survivor species.

Project description:Symbiotic microbial communities play key roles in the health and development of their multicellular hosts. Understanding why microbial communities vary among different host species or individuals is an important step toward understanding the diversity and function of the microbiome. The amphibian skin microbiome may affect resistance to the fungal pathogen Batrachochytrium dendrobatidis (Bd). Still, the factors that determine the diversity and composition of the amphibian skin microbiome, and therefore may ultimately contribute to disease resistance, are not well understood. We conducted a two-phase experiment to first test how host and environment shape the amphibian skin microbiome, and then test if the microbiome affects or is affected by Bd infection. Most lab experiments testing assembly of the amphibian skin microbiome so far have compared sterile to non-sterile environments or heavily augmented to non-augmented frogs. A goal of this study was to evaluate, in an experimental setting, realistic potential drivers of microbiome assembly that would be relevant to patterns observed in nature. We tested effects of frog genetic background (2 source populations) and 6 natural lake water sources in shaping the microbiome of the frog Rana sierrae. Water in which frogs were housed affected the microbiome in a manner that partially mimicked patterns observed in natural populations. In particular, frogs housed in water from disease-resistant populations had greater bacterial richness than frogs housed in water from populations that died out due to Bd. However, in the experiment this difference in microbiomes did not lead to differences in host mortality or rates of pathogen load increase. Frog source population also affected the microbiome and, although none of the frogs in this study showed true resistance to infection, host source population had a small effect on the rate of pathogen load increase. This difference in infection trajectories could be due to the observed differences in the microbiome, but could also be due to other traits that differ between frogs from the two populations. In addition to examining effects of the microbiome on Bd, we tested the effect of Bd infection severity on the microbiome. Specifically, we studied a time series of the microbiome over the course of infection to test if the effects of Bd on the microbiome are dependent on Bd infection severity. Although limited to a small subset of frogs, time series analysis suggested that relative abundances of several bacterial phylotypes changed as Bd loads increased through time, indicating that Bd-induced disturbance of the R. sierrae microbiome is not a binary effect but instead is dependent on infection severity. We conclude that both host and aquatic environment help shape the R. sierrae skin microbiome, with links to small changes in disease resistance in some cases, but in this study the effect of Bd on the microbiome was greater than the effect of the microbiome on Bd. Assessment of the microbiome differences between more distantly related populations than those studied here is needed to fully understand the role of the microbiome in resistance to Bd.

Project description:IntroductionTranslocation is a valuable and increasingly used strategy for the management of both threatened and overabundant wildlife populations. However, in some instances the translocated animals fail to thrive. Differences in diet between the source and destination areas may contribute to poor translocation outcomes, which could conceivably be exacerbated if the animals' microbiomes are unsuited to the new diet and cannot adapt.MethodsIn this study we tracked how the faecal microbiome of a specialist Eucalyptus folivore, the koala (Phascolarctos cinereus), changed over the course of a year after translocation. We assessed microbiome composition by 16S rRNA amplicon sequencing of faecal pellets.ResultsWe found no significant overall changes in the faecal microbiomes of koalas post-translocation (n = 17) in terms of microbial richness, diversity or composition when compared to the faecal microbiomes of koalas from an untranslocated control group (n = 12). This was despite the translocated koalas feeding on a greater variety of Eucalyptus species after translocation. Furthermore, while differences between koalas accounted for half of the microbiome variation, estimated diets at the time of sampling only accounted for 5% of the variation in the koala microbiomes between sampling periods. By contrast, we observed that the composition of koala faecal microbiomes at the time of translocation accounted for 37% of between koala variation in post-translocation diet. We also observed that translocated koalas lost body condition during the first month post-translocation and that the composition of the koalas' initial microbiomes were associated with the magnitude of that change.DiscussionThese findings suggest that the koala gut microbiome was largely unaffected by dietary change and support previous findings suggesting that the koala gut microbiome influences the tree species chosen for feeding. They further indicate that future research is needed to establish whether the koalas' gut microbiomes are directly influencing their health and condition or whether aspects of the koala gut microbiomes are an indicator of underlying physiological differences or pathologies. Our study provides insights into how animal microbiomes may not always be affected by the extreme upheaval of translocation and highlights that responses may be host species-specific. We also provide recommendations to improve the success of koala translocations in the future.

Project description:The soil microbiome represents one of the most complex microbial communities on the planet, encompassing thousands of taxa and metabolic pathways, rendering holistic analyses computationally intensive and difficult. Here, we developed an alternative approach in which the complex soil microbiome was broken into components ("functional modules"), based on metabolic capacities, for individual characterization. We hypothesized that reproducible, low-complexity communities that represent functional modules could be obtained through targeted enrichments and that, in combination, they would encompass a large extent of the soil microbiome diversity. Enrichments were performed on a starting soil inoculum with defined media based on specific carbon substrates, antibiotics, alternative electron acceptors under anaerobic conditions, or alternative growing conditions reflective of common field stresses. The resultant communities were evaluated through 16S rRNA amplicon sequencing. Less permissive modules (anaerobic conditions, complex polysaccharides, and certain stresses) resulted in more distinct community profiles with higher richness and more variability between replicates, whereas modules with simple substrates were dominated by fewer species and were more reproducible. Collectively, approximately 27% of unique taxa present in the liquid soil extract control were found across functional modules. Taxa that were underrepresented or undetected in the source soil were also enriched across the modules. Metatranscriptomic analyses were carried out on a subset of the modules to investigate differences in functional gene expression. These results demonstrate that by dissecting the soil microbiome into discrete components it is possible to obtain a more comprehensive view of the soil microbiome and its biochemical potential than would be possible using more holistic analyses.IMPORTANCE The taxonomic and functional diversity inherent to the soil microbiome complicate assessments of the metabolic potential carried out by the community members. An alternative approach is to break down the soil microbiome into reduced-complexity subsets based on metabolic capacities (functional modules) prior to sequencing and analysis. Here, we demonstrate that this approach successfully identified specific phylogenetic and biochemical traits of the soil microbiome that otherwise remained hidden from a more top-down analysis.

Dataset Information

Deconstructing the Bat Skin Microbiome: Influences of the Host and the Environment.

Publications

Deconstructing the Bat Skin Microbiome: Influences of the Host and the Environment.

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