Habitat disturbance influences the skin microbiome of a rediscovered neotropical-montane frog

Abstract

Background The skin microbiome serves as a first line defense against pathogens in vertebrates. In amphibians, it has the potential to protect against the chytrid fungus Batrachochytrium dendrobatis (Bd), a likely agent of amphibian declines. Alteration of the microbiome associated with unfavorable environmental changes produced by anthropogenic activities may make the host more susceptible to pathogens. Some amphibian species that were thought to be “extinct” have been rediscovered years after population declines in the late 1980s probably due to evolved Bd-resistance and are now threatened by anthropogenic land-use changes. Understanding the effects of habitat disturbance on the host skin microbiome is relevant for understanding the health of these species, along with its susceptibility to pathogens such as Bd. Here, we investigate the influence of habitat alteration on the skin bacterial communities as well as specifically the putative Bd-inhibitory bacterial communities of the montane frog Lithobates vibicarius. This species, after years of not being observed, was rediscovered in small populations inhabiting undisturbed and disturbed landscapes, and with continuous presence of Bd. Results We found that cutaneous bacterial communities of tadpoles and adults differed between undisturbed and disturbed habitats. The adults from disturbed habitats exhibited greater community dispersion than those from undisturbed habitats. We observed a higher richness of putative Bd-inhibitory bacterial strains in adults from disturbed habitats than in those from undisturbed habitats, as well as a greater number of these potential protective bacteria with a high relative abundance. Conclusions Our findings support the microbial “Anna Karenina principle”, in which disturbance is hypothesized to cause greater microbial dispersion in communities, a so-called dysbiosis, which is a response of animal microbiomes to stress factors that decrease the ability of the host or its microbiome to regulate community composition. On the positive side, the high richness and relative abundance of putative Bd-inhibitory bacteria may indicate the development of a defense mechanism that enhances Bd-protection, attributed to a co-occurrence of more than 30-years of host and pathogen in these disturbed habitats. Our results provide important insight into the influence of human-modified landscapes on the skin microbiome and health implications of Bd-survivor species.

Habitat Disturbance Linked with Host Microbiome Dispersion and Bd Dynamics in Temperate Amphibians

“…In this study, we use a Bd-enzootic system in the southeastern US to determine the in uences of habitat disturbance on microbiome-Bd dynamics. In line with recent studies [21,31,[36][37][38][39], we hypothesized that habitat disturbance and associated pond water physiochemistry would drive bacterial assembly in the environment, which together would shape composition of the amphibian skin microbiome. We proposed two contrasting predictions for how habitat disturbance would impact Bd: 1) disturbance could directly reduce Bd prevalence and infection loads by shifting optimal microclimates for Bd [48,49] or 2) disturbance could increase stochasticity in the microbiome, which could reduce host-protective effects of the microbial community and therefore indirectly increase Bd prevalence and loads.…”

“…This has been dubbed the "Anna Karenina principle", where microbiomes become more stochastic when organisms are under stress, leading to greater spread along principal component axes [31]. This principle is supported by recent studies on corals [18], anemones [36], frogs [21,37], and humans [38,39].…”

“…Amphibians often require multiple habitat types to complete their life cycle and are thus particularly responsive to anthropogenic habitat disturbances that may alter biotic and abiotic environmental conditions and in uence their movement. A recent study found that proximity to anthropogenic development was associated with higher dispersion and altered function of the microbiome of a neotropical frog species [37]. Recent work has also revealed associations between the composition of the amphibian skin microbiome and the outcome of infection with Batrachochytrium dendrobatidis (Bd), a waterborne fungal pathogen that is transmitted between hosts sharing the same habitat [26,30,[40][41][42][43][44].…”

A framework for testing the impact of co-infections on host gut microbiomes

“…Alternatively, dispersion may be seen as an evolutionary strategy to uncover an effective response from more divergent microbial communities (following similar principles behind host genetic diversity in relation to selection). The results of at least one study are suggestive: the skin microbiome of the recently re-discovered neotropical Green-eyed frog ( Lithobates vibicarius ) was more divergent among those individuals encountering frequent human disturbance [ 102 ]. The disturbed skin microbiome, however, was rich in bacteria with putative inhibitory function against the chytrid fungus Batrachochytrium dendrobatis ( Bd ), which drove the original decline of the species.…”

Characterization of the microbiome of the invasive Asian toad in Madagascar across the expansion range and comparison with a native co-occurring species

“…However, previous studies mostly included terrestrial amphibians (including P. mascarenienis ) from multiple habitats ( Bletz et al, 2017 ), while our study included only urban sites around Toamasina. This habitat is characterized by high anthropogenic pressures, such as the presence of cattle, human waste, no natural vegetation cover and poor availability of clean water bodies, that can potentially have impoverished the environmental bacterial pool and consequently reduced the richness of the bacterial communities in P. mascareniensis ( Becker et al, 2017 ; Jiménez et al, 2020 ) but this should be further investigated in future assessments.…”