Dataset Information

Diversity-Stability Dynamics of the Amphibian Skin Microbiome and Susceptibility to a Lethal Viral Pathogen.

ABSTRACT: Variation among animals in their host-associated microbial communities is increasingly recognized as a key determinant of important life history traits including growth, metabolism, and resistance to disease. Quantitative estimates of the factors shaping the stability of host microbiomes over time at the individual level in non-model organisms are scarce. Addressing this gap in our knowledge is important, as variation among individuals in microbiome stability may represent temporal gain or loss of key microbial species and functions linked to host health and/or fitness. Here we use controlled experiments to investigate how both heterogeneity in microbial species richness of the environment and exposure to the emerging pathogen Ranavirus influence the structure and temporal dynamics of the skin microbiome in a vertebrate host, the European common frog (Rana temporaria). Our evidence suggests that altering the bacterial species richness of the environment drives divergent temporal microbiome dynamics of the amphibian skin. Exposure to ranavirus effects changes in skin microbiome structure irrespective of total microbial diversity, but individuals with higher pre-exposure skin microbiome diversity appeared to exhibit higher survival. Higher diversity skin microbiomes also appear less stable over time compared to lower diversity microbiomes, but stability of the 100 most abundant ("core") community members was similar irrespective of microbiome richness. Our study highlights the importance of extrinsic factors in determining the stability of host microbiomes over time, which may in turn have important consequences for the stability of host-microbe interactions and microbiome-fitness correlations.

SUBMITTER: Harrison XA

PROVIDER: S-EPMC6951417 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Diversity-Stability Dynamics of the Amphibian Skin Microbiome and Susceptibility to a Lethal Viral Pathogen.

Harrison Xavier A XA Price Stephen J SJ Hopkins Kevin K Leung William T M WTM Sergeant Chris C Garner Trenton W J TWJ

Frontiers in microbiology 20191220

Variation among animals in their host-associated microbial communities is increasingly recognized as a key determinant of important life history traits including growth, metabolism, and resistance to disease. Quantitative estimates of the factors shaping the stability of host microbiomes over time at the individual level in non-model organisms are scarce. Addressing this gap in our knowledge is important, as variation among individuals in microbiome stability may represent temporal gain or loss ...[more]

PMID: 31956320

Similar Datasets

Project description:BackgroundThe fungal pathogen Batrachochytrium dendrobatidis (Bd) threatens amphibian biodiversity and ecosystem stability worldwide. Amphibian skin microbial community structure has been linked to the clinical outcome of Bd infections, yet its overall functional importance is poorly understood.MethodsMicrobiome taxonomic and functional profiles were assessed using high-throughput bacterial 16S rRNA and fungal ITS2 gene sequencing, bacterial shotgun metagenomics and skin mucosal metabolomics. We sampled 56 wild midwife toads (Alytes obstetricans) from montane populations exhibiting Bd epizootic or enzootic disease dynamics. In addition, to assess whether disease-specific microbiome profiles were linked to microbe-mediated protection or Bd-induced perturbation, we performed a laboratory Bd challenge experiment whereby 40 young adult A. obstetricans were exposed to Bd or a control sham infection. We measured temporal changes in the microbiome as well as functional profiles of Bd-exposed and control animals at peak infection.ResultsMicrobiome community structure and function differed in wild populations based on infection history and in experimental control versus Bd-exposed animals. Bd exposure in the laboratory resulted in dynamic changes in microbiome community structure and functional differences, with infection clearance in all but one infected animal. Sphingobacterium, Stenotrophomonas and an unclassified Commamonadaceae were associated with wild epizootic dynamics and also had reduced abundance in laboratory Bd-exposed animals that cleared infection, indicating a negative association with Bd resistance. This was further supported by microbe-metabolite integration which identified functionally relevant taxa driving disease outcome, of which Sphingobacterium and Bd were most influential in wild epizootic dynamics. The strong correlation between microbial taxonomic community composition and skin metabolome in the laboratory and field is inconsistent with microbial functional redundancy, indicating that differences in microbial taxonomy drive functional variation. Shotgun metagenomic analyses support these findings, with similar disease-associated patterns in beta diversity. Analysis of differentially abundant bacterial genes and pathways indicated that bacterial environmental sensing and Bd resource competition are likely to be important in driving infection outcomes.ConclusionsBd infection drives altered microbiome taxonomic and functional profiles across laboratory and field environments. Our application of multi-omics analyses in experimental and field settings robustly predicts Bd disease dynamics and identifies novel candidate biomarkers of infection. Video Abstract.

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.

Dataset Information

Diversity-Stability Dynamics of the Amphibian Skin Microbiome and Susceptibility to a Lethal Viral Pathogen.

Publications

Diversity-Stability Dynamics of the Amphibian Skin Microbiome and Susceptibility to a Lethal Viral Pathogen.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets