Abstract
Host-associated microbiotas of vertebrates are diverse and complex communities that contribute to host health. In particular, for amphibians, cutaneous microbial communities likely play a significant role in pathogen defense; however, our ecological understanding of these communities is still in its infancy. Here, we take advantage of the fully endemic and locally species-rich amphibian fauna of Madagascar to investigate the factors structuring amphibian skin microbiota on a large scale. Using amplicon-based sequencing, we evaluate how multiple host species traits and site factors affect host bacterial diversity and community structure. Madagascar is home to over 400 native frog species, all of which are endemic to the island; more than 100 different species are known to occur in sympatry within multiple rainforest sites. We intensively sampled frog skin bacterial communities, from over 800 amphibians from 89 species across 30 sites in Madagascar during three field visits, and found that skin bacterial communities differed strongly from those of the surrounding environment. Richness of bacterial operational taxonomic units (OTUs) and phylogenetic diversity differed among host ecomorphs, with arboreal frogs exhibiting lower richness and diversity than terrestrial and aquatic frogs. Host ecomorphology was the strongest factor influencing microbial community structure, with host phylogeny and site parameters (latitude and elevation) explaining less but significant portions of the observed variation. Correlation analysis and topological congruency analyses revealed little to no phylosymbiosis for amphibian skin microbiota. Despite the observed geographic variation and low phylosymbiosis, we found particular OTUs that were differentially abundant between particular ecomorphs. For example, the genus Pigmentiphaga (Alcaligenaceae) was significantly enriched on arboreal frogs, Methylotenera (Methylophilaceae) was enriched on aquatic frogs, and Agrobacterium (Rhizobiaceae) was enriched on terrestrial frogs. The presence of shared bacterial OTUs across geographic regions for selected host genera suggests the presence of core microbial communities which in Madagascar, might be driven more strongly by a species’ preference for specific microhabitats than by the physical, physiological or biochemical properties of their skin. These results corroborate that both host and environmental factors are driving community assembly of amphibian cutaneous microbial communities, and provide an improved foundation for elucidating their role in disease resistance.
Highlights
Mucosal environments of vertebrate hosts are inhabited by diverse microbial assemblages (Bäckhed et al, 2005; Rosenthal et al, 2011; Krediet et al, 2013; Brune and Dietrich, 2015; Colombo et al, 2015; Jiménez and Sommer, 2016)
Bacterial symbionts isolated from amphibian skin can inhibit Batrachochytrium dendrobatidis (Bd) growth through the production of anti-fungal compounds (Harris et al, 2006; Brucker et al, 2008a,b; Flechas et al, 2012; Woodhams et al, 2015), and population survival has been linked to the proportion of amphibians with Bd-inhibitory bacteria in the western United States (Lam et al, 2010)
Frog skin microbiotas were dominated by Proteobacteria (Gamma – 46.6%, Beta – 15.4%, Alpha – 9.4%, Delta – 1.6%), Bacteriodetes (8.1%), Actinobacteria (7.9%), Firmicutes
Summary
Mucosal environments of vertebrate hosts are inhabited by diverse microbial assemblages (Bäckhed et al, 2005; Rosenthal et al, 2011; Krediet et al, 2013; Brune and Dietrich, 2015; Colombo et al, 2015; Jiménez and Sommer, 2016). Amphibian skin hosts one of the best-studied wildlife microbiotas due to the role of these cutaneous microbial communities in meditating defense against the lethal pathogen, Batrachochytrium dendrobatidis (Bd) (Belden and Harris, 2007; Bletz et al, 2013; Jiménez and Sommer, 2016). These microbial communities provide a first line of defense against invading pathogens, such as Bd (Becker and Harris, 2010). Microbial therapies have been proposed as a possible disease mitigation strategy for combating chytridiomycosis (Bletz et al, 2013; Walke and Belden, 2016; Woodhams et al, 2016), and investigation of the basic ecological principles dictating skin microbial community structure on amphibians can inform the development and application of probiotic therapies
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