Environmental influences on and antimicrobial activity of the skin microbiota of Proceratophrys boiei (Amphibia, Anura) across forest fragments

Abstract

The composition of the skin microbiota of amphibians is related to the biology of host species and environmental microbial communities. In this system, the environment serves as a microbial source and can modulate the hosted community. When habitats are fragmented and the environment disturbed, changes in the structure of this microbial community are expected. One important potential consequence of fragmentation is a compromised protective function of the microbiota against pathogenic microorganisms. In this study, the skin microbiota of the amphibian Proceratophrys boiei was characterized, evaluated for relationships with environmental variables and environmental sources of microbial communities, and its diversity evaluated for frog populations from fragmented and continuous forests. In addition, the antimicrobial activity of this skin community was studied in frogs from both forest types. Culture methods and 16S rRNA high-throughput gene sequencing were used to characterize the microbial community and demonstrated that the skin microbiota of P. boiei is more closely related to the soil microbial communities than those inhabiting water bodies or fragment matrix, the unforested area around the forested fragment. The microbial diversity and abundance of P. boiei skin microbiota are different between continuous forests and fragments. This community is correlated with environmental variables, especially with temperature of microhabitat and distance to human dwelling. All individuals of P. boiei harbored bacteria capable of inhibiting the growth of pathogenic bacteria and different strains of the pathogenic fungus Batrachochytrium dendrobatidis, and a total of 27 bacterial genera were detected. The results of this study indicate that the persistence of populations of this species will need balanced and sustained interactions among host, microorganisms, and environment. K E Y W O R D Samphibian, antimicrobials, environmental microbes, fragmented forests, metabolites, skin microbiota 902 | de ASSIS et Al.

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

“…In addition, the relative abundance of certain bacterial taxa on the skin of both life stages differed between the two habitat types. These microbiome changes are congruent with other studies with different taxa assessing the effects of environmental changes (e.g., the gut microbiota of Darwin’s finches in the Galapagos islands [ 42 ]) [ 11 , 18 , 42 ]. It is known that human activities have an impact on the abiotic conditions of the environment affecting the diversity of host bacterial communities.…”

“…This means that it can threaten the survival of individuals and the growth of populations due to a cascade of negative health effects [ 10 – 13 ]. In fact, several recent studies have documented how skin and gut microbiomes from different wildlife species can be sensitive to habitat fragmentation and contaminants attributed to human activities [ 14 – 18 ].…”

Characterization of the Skin Cultivable Microbiota Composition of the Frog Pelophylax perezi Inhabiting Different Environments

“…The environment acts as a major driving force for host–microbe interactions [ 2 , 4 , 33 , 35 , 36 ]. In the present work, the composition of the skin cultivable microbiota of Perez’s frog was studied by cultivation methods.…”

“…Amphibians are a group of vertebrates that harbor a rich and diverse microbiome on their skin [ 1 , 2 , 3 ]. It has been shown that this cutaneous microbiota may play an important role as a complement to the innate immune system of amphibians, by acting as a physical barrier, through the production of antimicrobial substances or even by stimulating the host immune system [ 4 , 5 ]. Amphibians colonized all continents (except Antarctica) with more than 7000 species, known nowadays [ 6 , 7 ].…”

“…The establishment of the microbial skin community in amphibians is mainly obtained on the vertical transmission of parental microbes, horizontal transmission (e.g., during mating), pool of microbes present in the external environment (both aquatic and terrestrial), and on the interaction between the host’s immune system/mucous composition with bacteria [ 21 , 29 , 34 , 35 ]. Beyond this, the skin microbial community can be influenced by several biotic and abiotic environmental factors like chemical contamination [ 4 , 33 , 35 , 36 , 37 , 38 ]. However, the research about the influence of pollution on the skin microbiome composition is starting to understand how these changes are achieved.…”