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.

Amphibian ranaviruses in Europe: important directions for future research

“…Understanding the mechanism underlying microbiome-disease relationships Whilst present evidence represents an intriguing first demonstration of the potentially important role of the commensal microbiome for determining host response to ranavirosis, the mechanisms and directionality of this relationship are not understood (Campbell et al 2019;Harrison et al 2019). Particularly, it is unknown whether the composition of bacteria on amphibian skin is the result of originating from a population with endemic ranavirosis or whether certain bacterial community compositions can predispose a population to suffer outbreaks of ranavirosis.…”

“…Differing bacterial communities have been detected on the skin of frogs originating from populations with endemic ranavirosis versus frogs from populations with no history of disease, based on both transcriptomic (Campbell et al 2018b) and genomic DNA (Campbell et al 2019) sequences. Beyond these field-based studies, the outcome of acute ranaviral infection has been shown to be impacted by the diversity of the amphibian skin microbiome during an experimental study that showed that metamorphic R. temporaria with a depauperate bacterial microbiome were more likely to succumb to infection with FV3 than were metamorphic R. temporaria possessing a skin microbiome with higher species richness (Harrison et al 2019).…”

“…Although this evidence is primarily drawn from studies concerning amphibians infected with the chytrid fungi, including Batrachochytrium dendrobatidis (Bd) (Kueneman et al 2016; and B. salamandrivorans (Bates et al 2019), recent research suggests that host-associated microbial communities in amphibians also represent a key component of their immune defense against ranaviruses. For example, skin microbiome structure has been found to correlate with population disease-status in the wild (Campbell et al 2018b(Campbell et al , 2019 and survival of acute ranaviral infection under laboratory conditions (Harrison et al 2019). Furthermore, gut microbiomes of developing wood frogs (Rana sylvatica) have been shown to be critical modulators of later life resistance to ranavirus (Warne et al 2019).…”

“…Though a vast number of studies focus on drivers of microbiome structure in the wild, very few focus on microbiome stability and its consequences for the host. Recent experimental work has revealed that the stability of the amphibian skin microbiome is governed by the complexity of the environmental microbial reservoir (Harrison et al 2019). This gives us strong reason to expect that there is marked variation in the stability of the skin microbiome in wild frogs, which may even vary by population in concert with local environmental conditions.…”

“…Particularly, it is unknown whether the composition of bacteria on amphibian skin is the result of originating from a population with endemic ranavirosis or whether certain bacterial community compositions can predispose a population to suffer outbreaks of ranavirosis. Both ranavirosis (Harrison et al 2019) and chytridiomycosis (Jani and Briggs 2014) have been shown to perturb the amphibian skin microbiome, which could be expected to generate correlations between microbiome structure and disease status. Understanding the direction of this relationship is critical to appreciate the true potential of using probiotic treatments or bioaugmentation strategies to combat ranaviruses in wild populations.…”