Characterization of the Skin Microbiota in Italian Stream Frogs (<i>Rana italica</i>) Infected and Uninfected by a Cutaneous Parasitic Disease

Abstract

In human and wildlife populations, the natural microbiota plays an important role in health maintenance and the prevention of emerging infectious diseases. In amphibians, infectious diseases have been closely associated with population decline and extinction worldwide. Skin symbiont communities have been suggested as one of the factors driving the different susceptibilities of amphibians to diseases. The activity of the skin microbiota of amphibians against fungal pathogens, such as Batrachochytrium dendrobatidis, has been examined extensively, whereas its protective role towards the cutaneous infectious diseases caused by Amphibiocystidium parasites has not yet been elucidated in detail. In the present study, we investigated, for the first time, the cutaneous microbiota of the Italian stream frog (Rana italica) and characterized the microbial assemblages of frogs uninfected and infected by Amphibiocystidium using the Illumina next-generation sequencing of 16S rRNA gene fragments. A total of 629 different OTUs belonging to 16 different phyla were detected. Bacterial populations shared by all individuals represented only one fifth of all OTUs and were dominated by a small number of OTUs. Statistical analyses based on Bray-Curtis distances showed that uninfected and infected specimens had distinct cutaneous bacterial community structures. Phylotypes belonging to the genera Janthinobacterium, Pseudomonas, and Flavobacterium were more abundant, and sometimes almost exclusively present, in uninfected than in infected specimens. These bacterial populations, known to exhibit antifungal activity in amphibians, may also play a role in protection against cutaneous infectious diseases caused by Amphibiocystidium parasites.

Antifungal Bacteria on Woodland Salamander Skin Exhibit High Taxonomic Diversity and Geographic Variability

“…dendrobatidis bacteria likely have general antimicrobial properties (52) and may provide a general defensive benefit against pathogens to the host (9,13,23,42). Therefore, our results may also be useful if the deadly, closely related fungal pathogen Batrachochytrium salamandrivorans (43) reaches this salamander biodiversity hot spot (44).…”

“…Lower disease risk in vertebrates has been associated with different characteristics of the microbiome, such as high bacterial species richness (6)(7)(8), specific microbial community assemblages (2,7,9,10), and the presence of microbes that produce metabolites that inhibit growth of pathogens (1,11,12). For amphibians, inter-and intraspecies-specific variations in the skin microbiome (13)(14)(15) may contribute to variation in responses to infection by the deadly fungal pathogen Batrachochytrium dendrobatidis (16,17).…”

Ecological patterns in the skin microbiota of frogs from tropical Australia

“…() reported the numerical dominance of both Actinomycetales and Sphingomonadales on the skin of toads and their possible antifungal role. The Pseudomonadales, particularly those of the genus Pseudomonas , contain several species known to provide protection against pathogenic bacteria and fungi (Chang, Huang, Lin, Huang, & Liao, ; Federici et al., ). The Enterobacteriales were dominant in this study, and while this order has been reported from the guts of frogs (Chang et al., ), we found only two reports from amphibian (toad) skin studies (Hughey et al., ; Bataille et al.…”

“…Much of the research pertaining to frog skin microbiota has focused on the complexities of the epidemic of chytrid fungus (Rollins-Smith et al, 2011;Jani & Briggs, 2014;Holden et al, 2015;Berger et al, 2016;Bates et al, 2018) and other frog skin diseases (Federici et al, 2015;Knutie et al, 2017), including suggestions of using probiotics on frog populations (Harris et al, 2009;Loudon et al, 2014;Küng et al, 2014) even at a landscape scale (Muletz, Myers, Domangue, Herrick, & Harris, 2012). These efforts have yielded inconclusive results, including problems associated with the resilience of the skin microbiota inhibiting the uptake of probiotics (Küng et al, 2014).…”

Influence of immunogenetics, sex and body condition on the cutaneous microbial communities of two giant salamanders

“…Within amphibians, members of these families are commonly described as part of the skin microbiota (Jiménez & Sommer, ). However, Batrachochytrium dendrobatidis infection can induce a positive response in the abundance of Comamonadaceae , Flavobacteriaceae and Moraxellaceae (Federici et al., ; Jani & Briggs, ; Walke et al., ), and studies recording the effects of captivity on the skin of amphibians have recorded positive responses in members of these families as well (Becker et al. ).…”