Skin microbiome correlates with bioclimate and Batrachochytrium dendrobatidis infection intensity in Brazil’s Atlantic Forest treefrogs (original) (raw)
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PeerJ, 2019
The amphibian skin microbiome has been the focus of recent studies aiming to better understand the role of these microbial symbionts in host defense against disease. However, host-associated microbial communities are complex and dynamic, and changes in their composition and structure can influence their function. Understanding temporal variation of bacterial communities on amphibian skin is critical for establishing baselines from which to improve the development of mitigation techniques based on probiotic therapy and provides long-term host protection in a changing environment. Here, we investigated whether microbial communities on amphibian skin change over time at a single site. To examine this, we collected skin swabs from two pond-breeding species of treefrogs, Agalychnis callidryas and Dendropsophus ebraccatus, over 4 years at a single lowland tropical pond in Panamá. Relative abundance of operational taxonomic units (OTUs) based on 16S rRNA gene amplicon sequencing was used t...
Proceedings of the National Academy of Sciences of the United States of America, 2014
Symbiotic microbial communities may interact with infectious pathogens sharing a common host. The microbiome may limit pathogen infection or, conversely, an invading pathogen can disturb the microbiome. Documentation of such relationships during naturally occurring disease outbreaks is rare, and identifying causal links from field observations is difficult. This study documented the effects of an amphibian skin pathogen of global conservation concern [the chytrid fungus Batrachochytrium dendrobatidis (Bd)] on the skin-associated bacterial microbiome of the endangered frog, Rana sierrae, using a combination of population surveys and laboratory experiments. We examined covariation of pathogen infection and bacterial microbiome composition in wild frogs, demonstrating a strong and consistent correlation between Bd infection load and bacterial community composition in multiple R. sierrae populations. Despite the correlation between Bd infection load and bacterial community composition, ...
Host-associated microbial communities are ubiquitous among animals, and serve important functions. For example, the bacterial skin microbiome of amphibians can play a role in preventing or reducing infection by the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Evidence suggests that environmental bacteria likely serve as a source pool for at least some of the members of the amphibian skin bacterial community, underscoring the potential for local environmental changes to disrupt microbial community source pools that could be critical to the health of host organisms. However, few studies have assessed variation in the amphibian skin microbiome along clear environmental gradients, and so we know relatively little about how local environmental conditions influence microbiome diversity. We sampled the skin bacterial communities of Coqui frogs, Eleutherodactylus coqui (N = 77), along an elevational gradient in eastern Puerto Rico (0–875 m), with transects in two land use types: intact forest (N = 4 sites) and disturbed (N = 3 sites) forest. We found that alpha diversity (as assessed by Shannon, Simpson, and Phylogenetic Diversity indices) varied across sites, but this variation was not correlated with elevation or land use. Beta diversity (community structure), on the other hand, varied with site, elevation and land use, primarily due to changes in the relative abundance of certain bacterial OTUs (∼species) within these communities. Importantly, although microbiome diversity varied, E. coqui maintained a common core microbiota across all sites. Thus, our findings suggest that environmental conditions can influence the composition of the skin microbiome of terrestrial amphibians, but that some aspects of the microbiome remain consistent despite environmental variation.
Royal Society Open Science, 2015
Recently, microbiologists have focused on characterizing the probiotic role of skin bacteria for amphibians threatened by the fungal disease chytridiomycosis. However, the specific characteristics of microbial diversity required to maintain health or trigger disease are still not well understood in natural populations. We hypothesized that seasonal and developmental transitions affecting susceptibility to chytridiomycosis could also alter the stability of microbial assemblages. To test our hypothesis, we examined patterns of skin bacterial diversity in two species of declining amphibians ( Lithobates yavapaiensis and Eleutherodactylus coqui ) affected by the pathogenic fungus Batrachochytrium dendrobatidis ( Bd ). We focused on two important transitions that affect Bd susceptibility: ontogenetic (from juvenile to adult) shifts in E. coqui and seasonal (from summer to winter) shifts in L. yavapaiensis . We used a combination of community-fingerprinting analyses and 16S rRNA amplicon...
Fungal Ecology, 2021
Latitudinal gradients are linked to the dynamics of infectious diseases. Both prevalence and infection intensity of the amphibian-killing fungus, Batrachochytrium dendrobatidis (Bd), vary with latitude. Here, we tested whether abiotic and biotic factors are associated with Bd infection prevalence and intensity along a large latitudinal gradient across the Brazilian Atlantic Forest. We detected a positive association between infection prevalence and infection intensity with latitude; elevation, temperature and precipitation best explained infection prevalence, while temperature best explained infection intensity. We also detected a positive association between species richness and Bd infections and associations between Bd infections with host reproductive biology and habitat type. This represents the longest and most thoroughly sampled latitudinal gradient of Bd in anuran populations. Our results corroborate earlier findings that abiotic factors are a major determinant of Bd infections and highlight the need for a better understanding of the role that species diversity plays in disease outcomes.
The ISME Journal
Host-associated microbiomes are increasingly recognized to contribute to host disease resistance; the temporal dynamics of their community structure and function, however, are poorly understood. We investigated the cutaneous bacterial communities of three newt species, Ichthyosaura alpestris, Lissotriton vulgaris and Triturus cristatus, at approximately weekly intervals for 3 months using 16S ribosomal RNA amplicon sequencing. We hypothesized cutaneous microbiota would vary across time, and that such variation would be linked to changes in predicted fungal-inhibitory function. We observed significant temporal variation within the aquatic phase, and also between aquatic and terrestrial phase newts. By keeping T. cristatus in mesocosms, we demonstrated that structural changes occurred similarly across individuals, highlighting the non-stochastic nature of the bacterial community succession. Temporal changes were mainly associated with fluctuations in relative abundance rather than full turnover of bacterial operational taxonomic units (OTUs). Newt skin microbe fluctuations were not correlated with that of pond microbiota; however, a portion of community variation was explained by environmental temperature. Using a database of amphibian skin bacteria that inhibit the pathogen Batrachochytrium dendrobatidis (Bd), we found that the proportion of reads associated with 'potentially' Bd-inhibitory OTUs did not vary temporally for two of three newt species, suggesting that protective function may be maintained despite temporal variation in community structure.
Signatures of functional bacteriome structure in a tropical direct-developing amphibian species
Animal Microbiome
Background Host microbiomes may differ under the same environmental conditions and these differences may influence susceptibility to infection. Amphibians are ideal for comparing microbiomes in the context of disease defense because hundreds of species face infection with the skin-invading microbe Batrachochytrium dendrobatidis (Bd), and species richness of host communities, including their skin bacteria (bacteriome), may be exceptionally high. We conducted a landscape-scale Bd survey of six co-occurring amphibian species in Brazil’s Atlantic Forest. To test the bacteriome as a driver of differential Bd prevalence, we compared bacteriome composition and co-occurrence network structure among the six focal host species. Results Intensive sampling yielded divergent Bd prevalence in two ecologically similar terrestrial-breeding species, a group with historically low Bd resistance. Specifically, we detected the highest Bd prevalence in Ischnocnema henselii but no Bd detections in Haddadu...
Environmental and Host Effects on Skin Bacterial Community Composition in Panamanian Frogs
Frontiers in microbiology, 2018
Research on the amphibian skin microbiota has focused on identifying bacterial taxa that deter a pathogenic chytrid fungus, and on describing patterns of microbiota variation. However, it remains unclear how environmental variation affects amphibian skin bacterial communities, and whether the overall functional diversity of the amphibian skin microbiota is associated to such variation. We sampled skin microbial communities from one dendrobatoid frog species across an environmental gradient along the Panama Canal, and from three dendrobatoid frog species before and after the onset of the wet season in one site. We found frog skin microbial alpha diversity to be highest in frogs from sites with low soil pH, but no clear effect of the onset of the wet season. However, we found frog skin microbial community structure to be affected by soil pH and the onset of the wet season, which also resulted in a decrease in between-sample variation. Across the sampled frog species, bacterial functio...
Community richness of amphibian skin bacteria correlates with bioclimate at the global scale
Nature Ecology & Evolution
Animal-associated microbiomes are integral to host health, yet key biotic and abiotic factors that shape host-associated microbial communities at the global scale remain poorly understood. We investigated global patterns in amphibian skin bacterial communities, incorporating samples from 2,349 individuals representing 205 amphibian species across a broad biogeographic range. We analyzed how biotic and abiotic factors correlate with skin microbial communities using multiple statistical approaches. Global amphibian skin bacterial richness was consistently correlated with temperature-associated factors. We found more diverse skin microbiomes in environments with colder winters and less stable thermal conditions, compared to environments with warm winters and less annual temperature variation. We used bioinformatically predicted bacterial growth rates, dormancy genes, and antibiotic synthesis genes, as well as inferred bacterial thermal growth optima to propose mechanistic hypotheses that may explain the observed patterns. We conclude that temporal and spatial characteristics of the host's macro-environment mediate microbial diversity.
Panamanian frog species host unique skin bacterial communities
Frontiers in Microbiology, 2015
Vertebrates, including amphibians, host diverse symbiotic microbes that contribute to host disease resistance. Globally, and especially in montane tropical systems, many amphibian species are threatened by a chytrid fungus, Batrachochytrium dendrobatidis (Bd), that causes a lethal skin disease. Bd therefore may be a strong selective agent on the diversity and function of the microbial communities inhabiting amphibian skin. In Panamá, amphibian population declines and the spread of Bd have been tracked. In 2012, we completed a field survey in Panamá to examine frog skin microbiota in the context of Bd infection. We focused on three frog species and collected two skin swabs per frog from a total of 136 frogs across four sites that varied from west to east in the time since Bd arrival. One swab was used to assess bacterial community structure using 16S rRNA amplicon sequencing and to determine Bd infection status, and one was used to assess metabolite diversity, as the bacterial production of anti-fungal metabolites is an important disease resistance function. The skin microbiota of the three Panamanian frog species differed in OTU (operational taxonomic unit, ∼bacterial species) community composition and metabolite profiles, although the pattern was less strong for the metabolites. Comparisons between frog skin bacterial communities from Panamá and the US suggest broad similarities at the phylum level, but key differences at lower taxonomic levels. In our field survey in Panamá, across all four sites, only 35 individuals (∼26%) were Bd infected. There was no clustering of OTUs or metabolite profiles based on Bd infection status and no clear pattern of west-east changes in OTUs or metabolite profiles across the four sites. Overall, our field survey data suggest that different bacterial communities might be producing broadly similar sets of metabolites across frog hosts and sites. Community structure and function may not be as tightly coupled in these skin symbiont microbial systems as it is in many macro-systems.