Dataset Information

Genetic variability and ontogeny predict microbiome structure in a disease-challenged montane amphibian.

ABSTRACT: Amphibian populations worldwide are at risk of extinction from infectious diseases, including chytridiomycosis caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Amphibian cutaneous microbiomes interact with Bd and can confer protective benefits to the host. The composition of the microbiome itself is influenced by many environment- and host-related factors. However, little is known about the interacting effects of host population structure, genetic variation and developmental stage on microbiome composition and Bd prevalence across multiple sites. Here we explore these questions in Amietia hymenopus, a disease-affected frog in southern Africa. We use microsatellite genotyping and 16S amplicon sequencing to show that the microbiome associated with tadpole mouthparts is structured spatially, and is influenced by host genotype and developmental stage. We observed strong genetic structure in host populations based on rivers and geographic distances, but this did not correspond to spatial patterns in microbiome composition. These results indicate that demographic and host genetic factors affect microbiome composition within sites, but different factors are responsible for host population structure and microbiome structure at the between-site level. Our results help to elucidate complex within- and among- population drivers of microbiome structure in amphibian populations. That there is a genetic basis to microbiome composition in amphibians could help to inform amphibian conservation efforts against infectious diseases.

SUBMITTER: Griffiths SM

PROVIDER: S-EPMC6155040 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Genetic variability and ontogeny predict microbiome structure in a disease-challenged montane amphibian.

Griffiths Sarah M SM Harrison Xavier A XA Weldon Ché C Wood Michael D MD Pretorius Abigail A Hopkins Kevin K Fox Graeme G Preziosi Richard F RF Antwis Rachael E RE

The ISME journal 20180625 10

Amphibian populations worldwide are at risk of extinction from infectious diseases, including chytridiomycosis caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Amphibian cutaneous microbiomes interact with Bd and can confer protective benefits to the host. The composition of the microbiome itself is influenced by many environment- and host-related factors. However, little is known about the interacting effects of host population structure, genetic variation and developmental st ...[more]

PMID: 29942072

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Project description:BACKGROUND:Understanding the underlying processes shaping spatial patterns of genetic structure in free-ranging organisms is a central topic in evolutionary biology. Here, we aim to disentangle the relative importance of neutral (i.e. genetic drift) and local adaptation (i.e. ecological divergence) processes in the evolution of spatial genetic structure of the Morales grasshopper (Chorthippus saulcyi moralesi), a narrow-endemic taxon restricted to the Central Pyrenees. More specifically, we analysed range-wide patterns of genetic structure and tested whether they were shaped by geography (isolation-by-distance, IBD), topographic complexity and present and past habitat suitability models (isolation-by-resistance, IBR), and environmental dissimilarity (isolation-by-environment, IBE). RESULTS:Different clustering analyses revealed a deep genetic structure that was best explained by IBR based on topographic complexity. Our analyses did not reveal a significant role of IBE, a fact that may be due to low environmental variation among populations and/or consequence of other ecological factors not considered in this study are involved in local adaptation processes. IBR scenarios informed by current and past climate distribution models did not show either a significant impact on genetic differentiation after controlling for the effects of topographic complexity, which may indicate that they are not capturing well microhabitat structure in the present or the genetic signal left by dispersal routes defined by habitat corridors in the past. CONCLUSIONS:Overall, these results indicate that spatial patterns of genetic variation in our study system are primarily explained by neutral divergence and migration-drift equilibrium due to limited dispersal across abrupt reliefs, whereas environmental variation or spatial heterogeneity in habitat suitability associated with the complex topography of the region had no significant effect on genetic discontinuities after controlling for geography. Our study highlights the importance of considering a comprehensive suite of potential isolating mechanisms and analytical approaches in order to get robust inferences on the processes promoting genetic divergence of natural populations.

Project description:BackgroundMajor advances over the past decade in molecular ecology are providing access to soil fungal diversity in forest ecosystems worldwide, but the diverse functions and metabolic capabilities of this microbial community remain largely elusive. We conducted a field survey in montane old-growth broadleaved and conifer forests, to investigate the relationship between soil fungal diversity and functional genetic traits. To assess the extent to which variation in community composition was associated with dominant tree species (oak, spruce, and fir) and environmental variations in the old-growth forests in the Jade Dragon Snow Mountain in Yunnan Province, we applied rDNA metabarcoding. We also assessed fungal gene expression in soil using mRNA sequencing and specifically assessed the expression of genes related to organic matter decomposition and nutrient acquisition in ectomycorrhizal and saprotrophic fungi.ResultsOur taxonomic profiling revealed striking shifts in the composition of the saprotrophic and ectomycorrhizal guilds among the oak-, fir-, and spruce-dominated forests. The core fungal microbiome comprised only ~ 20% of the total OTUs across all soil samples, although the overlap between conifer-associated communities was substantial. In contrast, seasonality and soil layer explained only a small proportion of the variation in community structure. However, despite their highly variable taxonomic composition, fungal guilds exhibited remarkably similar functional traits for growth-related and core metabolic pathways across forest associations, suggesting ecological redundancy. However, we found that the expression profiles of genes related to polysaccharide and protein degradation and nutrient transport notably varied between and within the fungal guilds, suggesting niche adaptation.ConclusionsOverall, our metatranscriptomic analyses revealed the functional potential of soil fungal communities in montane old-growth forests, including a suite of specialized genes and taxa involved in organic matter decomposition. By linking genes to ecological traits, this study provides insights into fungal adaptation strategies to biotic and environmental factors, and sheds light on the importance of understanding functional gene expression patterns in predicting ecosystem functioning. Video Abstract.

Project description:Pathogenesis is strongly dependent on microbial context, but development of probiotic therapies has neglected the impact of ecological interactions. Dynamics among microbial communities, host immune responses, and environmental conditions may alter the effect of probiotics in human and veterinary medicine, agriculture and aquaculture, and the proposed treatment of emerging wildlife and zoonotic diseases such as those occurring on amphibians or vectored by mosquitoes. Here we use a holistic measure of amphibian mucosal defenses to test the effects of probiotic treatments and to assess disease risk under different ecological contexts. We developed a non-invasive assay for antifungal function of the skin mucosal ecosystem (mucosome function) integrating host immune factors and the microbial community as an alternative to pathogen exposure experiments. From approximately 8500 amphibians sampled across Europe, we compared field infection prevalence with mucosome function against the emerging fungal pathogen Batrachochytrium dendrobatidis. Four species were tested with laboratory exposure experiments, and a highly susceptible species, Alytes obstetricans, was treated with a variety of temperature and microbial conditions to test the effects of probiotic therapies and environmental conditions on mucosome function. We found that antifungal function of the amphibian skin mucosome predicts the prevalence of infection with the fungal pathogen in natural populations, and is linked to survival in laboratory exposure experiments. When altered by probiotic therapy, the mucosome increased antifungal capacity, while previous exposure to the pathogen was suppressive. In culture, antifungal properties of probiotics depended strongly on immunological and environmental context including temperature, competition, and pathogen presence. Functional changes in microbiota with shifts in temperature provide an alternative mechanistic explanation for patterns of disease susceptibility related to climate beyond direct impact on host or pathogen. This nonlethal management tool can be used to optimize and quickly assess the relative benefits of probiotic therapies under different climatic, microbial, or host conditions.

Dataset Information

Genetic variability and ontogeny predict microbiome structure in a disease-challenged montane amphibian.

Publications

Genetic variability and ontogeny predict microbiome structure in a disease-challenged montane amphibian.

Similar Datasets

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