Amphibian skin may select for rare environmental microbes

Abstract

Host-microbe symbioses rely on the successful transmission or acquisition of symbionts in each new generation. Amphibians host a diverse cutaneous microbiota, and many of these symbionts appear to be mutualistic and may limit infection by the chytrid fungus, Batrachochytrium dendrobatidis, which has caused global amphibian population declines and extinctions in recent decades. Using bar-coded 454 pyrosequencing of the 16S rRNA gene, we addressed the question of symbiont transmission by examining variation in amphibian skin microbiota across species and sites and in direct relation to environmental microbes. Although acquisition of environmental microbes occurs in some host-symbiont systems, this has not been extensively examined in free-living vertebrate-microbe symbioses. Juvenile bullfrogs (Rana catesbeiana), adult red-spotted newts (Notophthalmus viridescens), pond water and pond substrate were sampled at a single pond to examine host-specificity and potential environmental transmission of microbiota. To assess population level variation in skin microbiota, adult newts from two additional sites were also sampled. Cohabiting bullfrogs and newts had distinct microbial communities, as did newts across the three sites. The microbial communities of amphibians and the environment were distinct; there was very little overlap in the amphibians' core microbes and the most abundant environmental microbes, and the relative abundances of OTUs that were shared by amphibians and the environment were inversely related. These results suggest that, in a host species-specific manner, amphibian skin may select for microbes that are generally in low abundance in the environment.

Inhibitory bacteria reduce fungi on early life stages of endangered Colorado boreal toads (Anaxyrus boreas)

“…Our knowledge of amphibian skin microbiomes is rapidly increasing (Jani and Briggs, 2014;Kueneman et al, 2014;Walke et al, 2014). Exploring skin bacterial communities across different amphibian developmental stages and the defensive functions those microbes play, particularly prior to the development of the adaptive immune function, is an important and understudied area.…”

“…Consequently, skin-associated microbial communities and the innate immune system may serve as the primary lines of defense against pathogens for larval amphibians before the adaptive immune system is fully functional. The mechanisms underlying how host species select and maintain bacterial communities on the skin are not yet fully understood (Walke et al, 2014), but host immune systems mediate microbial interactions in many ways (Tennessen et al, 2009). In amphibians, mucus glands produce secretions that act as a physical protective barrier and substrate for resident microbiota (Rollins-Smith et al, 2009;Woodhams et al, 2014).…”

Short-Term Exposure to Coal Combustion Waste Has Little Impact on the Skin Microbiome of Adult Spring Peepers (Pseudacris crucifer)

“…From this research, it is clear that amphibians host a diverse group of symbiotic microbes on their skin (28,29). Many of these microbial symbionts are found in amphibian habitats, suggesting an environmental origin (29,30); furthermore, environmental source pools appear to be important for the maintenance of the amphibian skin microbiome (31). To begin to examine the potential impacts of fly ash on microbial communities in general and on the amphibian skin microbiome, we assessed bacterial communities in substrate and in water from reference and fly ash-contaminated wetlands where amphibians breed.…”

“…In the last decade, research on the amphibian microbiome has also increased, mainly in relation to the potential protective role of the skin microbiome in defense against the lethal skin pathogen Batrachochytrium dendrobatidis (25)(26)(27). From this research, it is clear that amphibians host a diverse group of symbiotic microbes on their skin (28,29). Many of these microbial symbionts are found in amphibian habitats, suggesting an environmental origin (29,30); furthermore, environmental source pools appear to be important for the maintenance of the amphibian skin microbiome (31).…”

The pathogenBatrachochytrium dendrobatidisdisturbs the frog skin microbiome during a natural epidemic and experimental infection

“…A second knowledge gap is the paucity of comprehensive culture-independent assessments of the amphibian microbiome, which are important because the vast majority of environmental and symbiotic microbes are not readily cultured, and culture-based methods can lead to severe underestimates of diversity and biased assessment of community composition (43). Few studies have applied next-generation sequencing methods to characterize the microbial communities on amphibian skin (44)(45)(46)(47), and, to our knowledge, none have done so in the context of Bd infection. A final challenge to understanding interactions between Bd and bacteria stems from the difficulties of drawing direct connections between laboratory and field studies.…”