Collaborative Research: Linking Causes of Variation in the Amphibian Skin Microbiome with Consequences for Disease Risk

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Animals have communities of microbes (bacteria, viruses, fungi) living in and on their bodies. These microbial communities are referred to as symbiotic microbial communities, or the microbiome. Symbiotic microbial communities are increasingly recognized as important players in the health of humans and animals. Symbiotic microbes may be important to animal (host) health by affecting host response to disease-causing organisms (pathogens). This project aims to understand how the microbiome affects disease resistance while studying chytridiomycosis, a devastating disease of amphibians (frogs, toads and salamanders) caused by the pathogen Batrachochytrium dendrobatidis (abbreviated Bd). Bd is a fungus that infects the skin of amphibians and can cause potentially-lethal chytridiomycosis. The Sierra Nevada yellow-legged frog (Rana sierrae) is in danger of extinction and Bd is one of the most serious threats to this frog. Bd has caused massive die-offs of entire populations of R. sierrae. However, certain populations of R. sierrae appear to be somewhat resistant to lethal chytridiomycosis. Understanding why these resistant populations are able to survive despite Bd infection may be critical for efforts to conserve the species. It is possible that the skin microbiome contributes to disease resistance, however definitive evidence is lacking. This project will address three core questions: (1) To what extent does the R. sierrae skin microbiome contribute to disease resistance? (2) Does microbiome composition (i.e., the microbial species that make up the microbiome) affect the stability of the microbiome when frogs become infected with Bd? This may be important to understanding continued functionality of the microbiome when the host is threatened by infectious diseases. (3) How do host and environmental differences affect microbiome assembly? In other words, what are the forces that lead to differences in the microbiome of different frogs or populations, or within an individual frog at different times? This may reveal underlying causes that shape functional variation attributed to the microbiome, such as differences in disease resistance. In summary, this work will advance understanding of how host and environment determine microbiome composition and how this in turn may shape microbiome function and stability. Understanding of these processes is relevant to strategies for protecting threatened amphibians. More broadly, understanding how the R. sierrae microbiome interacts with Bd can provide insights into microbiome-pathogen interactions and management of infectious disease in other animals and humans.Symbiotic microbial communities are increasingly recognized as important players in the development and health of multicellular organisms. Several studies have found that disease caused by pathogenic microbes is associated with changes in the composition of the microbiome of the host compared with the microflora of healthy individuals, but it has often been difficult to determine cause and effect: the observed correlation may indicate that particular microbiome assemblages confer disease resistance, or that pathogen infection disrupts and alters the microbiome. This project aims to understand the role of the amphibian skin-associated bacterial community (skin microbiome) in mediating resistance to the fungal pathogen Batrachochytrium dendrobatidis. The project will test if microbiome differences exist between disease-resistant and -susceptible hosts, suggestive of a protective role in nature. Importantly, this work will further clarify the causal relationship between pathogen and microbiome by testing if experimental alteration of the microbiome leads to changes in disease resistance, or if instead pathogen infection alters the microbiome. This study also aims to understand what determines the phylogenetic and functional composition of the microbiome, a question that is fundamental to understanding the root of microbiome-associated differences in disease resistance. Field surveys will be used to quantify the degree to which host genetic variation and environmental factors are associated with the phylogenetic and functional composition of the skin microbiome sampled from wild frogs, while experimental manipulations will clearly show cause and effect in these relationships. Mathematical models will be developed to identify ecological mechanisms that potentially drive variation in microbial community composition. Finally, predictive models of microbial community dynamics under conditions of disturbance (such as pathogen infection) will be developed, integrating community assembly and disease resistance concepts.