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Title: Effects of grassland controlled burning on symbiotic skin microbes in Neotropical amphibians
Climate change has led to an alarming increase in the frequency and severity of wildfires worldwide. While it is known that amphibians have physiological characteristics that make them highly susceptible to fire, the specific impacts of wildfires on their symbiotic skin bacterial communities (i.e., bacteriomes) and infection by the deadly chytrid fungus, Batrachochytrium dendrobatidis, remain poorly understood. Here, we address this research gap by evaluating the effects of fire on the amphibian skin bacteriome and the subsequent risk of chytridiomycosis. We sampled the skin bacteriome of the Neotropical species Scinax squalirostris and Boana leptolineata in fire and control plots before and after experimental burnings. Fire was linked with a marked increase in bacteriome beta dispersion, a proxy for skin microbial dysbiosis, alongside a trend of increased pathogen loads. By shedding light on the effects of fire on amphibian skin bacteriomes, this study contributes to our broader understanding of the impacts of wildfires on vulnerable vertebrate species. more »« less
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 microbeBatrachochytrium 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 inIschnocnema henseliibut no Bd detections inHaddadus binotatus.Haddadus binotatuscarried the highest bacteriome alpha and common core diversity, and a modular network partitioned by negative co-occurrences, characteristics associated with community stability and competitive interactions that could inhibit Bd colonization.
Conclusions
Our findings suggest that community structure of the bacteriome might drive Bd resistance inH. binotatus, which could guide microbiome manipulation as a conservation strategy to protect diverse radiations of direct-developing species from Bd-induced population collapses.
Abstract Microbial diversity positively influences community resilience of the host microbiome. However, extinction risk factors such as habitat specialization, narrow environmental tolerances, and exposure to anthropogenic disturbance may homogenize host-associated microbial communities critical for stress responses including disease defense. In a dataset containing 43 threatened and 90 non-threatened amphibian species across two biodiversity hotspots (Brazil’s Atlantic Forest and Madagascar), we found that threatened host species carried lower skin bacterial diversity, after accounting for key environmental and host factors. The consistency of our findings across continents suggests the broad scale at which low bacteriome diversity may compromise pathogen defenses in species already burdened with the threat of extinction.
Fire strongly affects animals’ behavior, population dynamics, and environmental surroundings, which in turn are likely to affect their immune systems and exposure to pathogens. However, little work has yet been conducted on the effects of wildfires on wildlife disease. This research gap is rapidly growing in importance because wildfires are becoming globally more common and more severe, with unknown impacts on wildlife disease and unclear implications for livestock and human health in the future.
Results
Here, we discussed how wildfires could influence susceptibility and exposure to infection in wild animals, and the potential consequences for ecology and public health. In our framework, we outlined how habitat loss and degradation caused by fire affect animals’ immune defenses, and how behavioral and demographic responses to fire affect pathogen exposure, spread, and maintenance. We identified relative unknowns that might influence disease dynamics in unpredictable ways (e.g., through altered community composition and effects on free-living parasites). Finally, we discussed avenues for future investigations of fire-disease links.
Conclusions
We hope that this review will stimulate much-needed research on the role of wildfire in influencing wildlife disease, providing an important source of information on disease dynamics in the wake of future wildfires and other natural disasters, and encouraging further integration of the fields of fire and disease ecology.
Gajewski, Zachary; Johnson, Leah R.; Medina, Daniel; Crainer, William W.; Nagy, Christopher M.; Belden, Lisa K.(
, PeerJ)
Skin microbial communities are an essential part of host health and can play a role in mitigating disease. Host and environmental factors can shape and alter these microbial communities and, therefore, we need to understand to what extent these factors influence microbial communities and how this can impact disease dynamics. Microbial communities have been studied in amphibian systems due to skin microbial communities providing some resistance to the amphibian chytrid fungus, Batrachochytrium dendrobatidis . However, we are only starting to understand how host and environmental factors shape these communities for amphibians. In this study, we examined whether amphibian skin bacterial communities differ among host species, host infection status, host developmental stage, and host habitat. We collected skin swabs from tadpoles and adults of three Ranid frog species ( Lithobates spp.) at the Mianus River Gorge Preserve in Bedford, New York, USA, and used 16S rRNA gene amplicon sequencing to determine bacterial community composition. Our analysis suggests amphibian skin bacterial communities change across host developmental stages, as has been documented previously. Additionally, we found that skin bacterial communities differed among Ranid species, with skin communities on the host species captured in streams or bogs differing from the communities of the species captured on land. Thus, habitat use of different species may drive differences in host-associated microbial communities for closely-related host species.
Amphibian population declines caused by the fungusBatrachochytrium dendrobatidis(Bd) have prompted studies on the bacterial community that resides on amphibian skin. However, studies addressing the fungal portion of these symbiont communities have lagged behind. Using ITS1 amplicon sequencing, we examined the fungal portion of the skin microbiome of temperate and tropical amphibian species currently coexisting with Bd in nature. We assessed cooccurrence patterns between bacterial and fungal OTUs using a subset of samples for which bacterial 16S rRNA gene amplicon data were also available. We determined that fungal communities were dominated by members of the phyla Ascomycota and Basidiomycota, and also by Chytridiomycota in the most aquatic amphibian species. Alpha diversity of the fungal communities differed across host species, and fungal community structure differed across species and regions. However, we did not find a correlation between fungal diversity/community structure and Bd infection, though we did identify significant correlations between Bd and specific OTUs. Moreover, positive bacterial–fungal cooccurrences suggest that positive interactions between these organisms occur in the skin microbiome. Understanding the ecology of amphibian skin fungi, and their interactions with bacteria will complement our knowledge of the factors influencing community assembly and the overall function of these symbiont communities.
Schuck, Laura K., Neely, Wesley J., Buttimer, Shannon M., Moser, Camila F., Barth, Priscila C., Liskoski, Paulo E., Caberlon, Carolina de, Valiati, Victor Hugo, Tozetti, Alexandro M., and Becker, C. Guilherme. Effects of grassland controlled burning on symbiotic skin microbes in Neotropical amphibians. Retrieved from https://par.nsf.gov/biblio/10486324. Scientific Reports 14.1 Web. doi:10.1038/s41598-023-50394-9.
Schuck, Laura K., Neely, Wesley J., Buttimer, Shannon M., Moser, Camila F., Barth, Priscila C., Liskoski, Paulo E., Caberlon, Carolina de, Valiati, Victor Hugo, Tozetti, Alexandro M., & Becker, C. Guilherme. Effects of grassland controlled burning on symbiotic skin microbes in Neotropical amphibians. Scientific Reports, 14 (1). Retrieved from https://par.nsf.gov/biblio/10486324. https://doi.org/10.1038/s41598-023-50394-9
Schuck, Laura K., Neely, Wesley J., Buttimer, Shannon M., Moser, Camila F., Barth, Priscila C., Liskoski, Paulo E., Caberlon, Carolina de, Valiati, Victor Hugo, Tozetti, Alexandro M., and Becker, C. Guilherme.
"Effects of grassland controlled burning on symbiotic skin microbes in Neotropical amphibians". Scientific Reports 14 (1). Country unknown/Code not available: Springer Nature. https://doi.org/10.1038/s41598-023-50394-9.https://par.nsf.gov/biblio/10486324.
@article{osti_10486324,
place = {Country unknown/Code not available},
title = {Effects of grassland controlled burning on symbiotic skin microbes in Neotropical amphibians},
url = {https://par.nsf.gov/biblio/10486324},
DOI = {10.1038/s41598-023-50394-9},
abstractNote = {Climate change has led to an alarming increase in the frequency and severity of wildfires worldwide. While it is known that amphibians have physiological characteristics that make them highly susceptible to fire, the specific impacts of wildfires on their symbiotic skin bacterial communities (i.e., bacteriomes) and infection by the deadly chytrid fungus, Batrachochytrium dendrobatidis, remain poorly understood. Here, we address this research gap by evaluating the effects of fire on the amphibian skin bacteriome and the subsequent risk of chytridiomycosis. We sampled the skin bacteriome of the Neotropical species Scinax squalirostris and Boana leptolineata in fire and control plots before and after experimental burnings. Fire was linked with a marked increase in bacteriome beta dispersion, a proxy for skin microbial dysbiosis, alongside a trend of increased pathogen loads. By shedding light on the effects of fire on amphibian skin bacteriomes, this study contributes to our broader understanding of the impacts of wildfires on vulnerable vertebrate species.},
journal = {Scientific Reports},
volume = {14},
number = {1},
publisher = {Springer Nature},
author = {Schuck, Laura K. and Neely, Wesley J. and Buttimer, Shannon M. and Moser, Camila F. and Barth, Priscila C. and Liskoski, Paulo E. and Caberlon, Carolina de and Valiati, Victor Hugo and Tozetti, Alexandro M. and Becker, C. Guilherme},
}
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