Microbiome Variation Across Amphibian Skin Regions: Implications for Chytridiomycosis Mitigation Efforts

Abstract

Cutaneous bacteria may play an important role in the resistance of amphibians to the pathogenic fungus Batrachochytrium dendrobatidis (Bd). Microbial communities resident on hosts' skin show topographical diversity mapping to skin features, as demonstrated by studies of the human microbiome. We examined skin microbiomes of wild and captive fire-bellied toads (Bombina orientalis) for differences across their body surface. We found that bacterial communities differed between ventral and dorsal skin. Wild toads showed slightly higher bacterial richness and diversity in the dorsal compared to the ventral region. On the other hand, captive toads hosted a higher richness and diversity of bacteria on their ventral than their dorsal skin. Microbial community composition and relative abundance of major bacterial taxonomic groups also differed between ventral and dorsal skin in all populations. Furthermore, microbiome diversity patterns varied as a function of their Bd infection status in wild toads. Bacterial richness and diversity was greater, and microbial community structure more complex, in wild than captive toads. The results suggest that bacterial community structure is influenced by microhabitats associated with skin regions. These local communities may be differentially modified when interacting with environmental bacteria and Bd. A better understanding of microbiome variation across skin regions will be needed to assess how the skin microbiota affects the abilities of amphibian hosts to resist Bd infection, especially in captive breeding programs.

The cutaneous ecosystem: the roles of the skin microbiome in health and its association with inflammatory skin conditions in humans and animals

“…In exotic species, most NGS studies have focused on characterizing the skin microbiota of amphibians . The most common phylotypes colonizing their skin include Bacteroidetes, Proteobacteria, Firmicutes and Sphingobacteria (Table ).…”

“…One study found that different amphibian species were strong predictors of microbial community composition and wetland sites explained significant variations across the same species of amphibians . Furthermore, another study found wild toads had greater bacterial richness and diversity than captive toads …”

“…The chytrid fungus Batrachochytrium dendrobatidis (Bd) has been studied extensively due to severe cutaneous infections resulting in marked mortality in several amphibian species and raising serious concerns especially to endangered amphibian species. Due to its severity, a few studies were developed to better understand the interactions between this fungus with the skin microbiota . One study demonstrated that Bd infection caused significant changes to the bacterial microbiota inhabiting the skin (Table ).…”

Evolutionary Biology Needs Wild Microbiomes

“…But captivity alters the microbiome in mammals (Uenishi et al, 2007; Delsuc et al, 2014; Kreisinger et al, 2014; Clayton et al, 2016; Delport et al, 2016), birds (Scupham et al, 2008; Matsui et al, 2010; Wienemann et al, 2011; Rodríguez-Ruano et al, 2015; Wang et al, 2016), fish (Dhanasiri et al, 2010), reptiles (Keenan et al, 2013), and amphibians (Loudon et al, 2013; Becker et al, 2014; Bataille et al, 2016), which is likely due to the dietary, social, and environmental conditions of captivity that are so different from those experienced in the wild. Captive microbiomes likely do not represent the natural variation of the microbiome of a species (or population), which is necessary for evolutionary analysis.…”

Skin bacterial microflora of two closely related mountain newts (Salamandridae) – the Yellow‐spotted mountain newt Neurergus derjugini and the Kaiser's mountain newt Neurergus kaiseri – in the wild and in a breeding facility highlight new conservation perspectives

“…However, the microbiome may also have an indirect influence on host health during interactions with infectious pathogens (Turnbaugh et al , ; Heijtz et al , ; Honda & Littman, ; Theis et al , ; Jani & Briggs, ). All amphibians show an important and diverse microbiota community on their permeable skin, which is thin and sensitive to their environment (Duellman & Trueb, ; Bataille et al , ). Amphibian species are mainly habitat specialists inhabiting specific ecological niches associated with water and humidity (Hernandez, ).…”