scholarly journals Host and Aquatic Environment Shape the Amphibian Skin Microbiome but Effects on Downstream Resistance to the Pathogen Batrachochytrium dendrobatidis Are Variable

2018 ◽  
Vol 9 ◽  
Author(s):  
Andrea J. Jani ◽  
Cheryl J. Briggs
2021 ◽  
Vol 1 (1) ◽  
pp. 26-37
Author(s):  
Randall R. Jiménez ◽  
Gilbert Alvarado ◽  
Clemens Ruepert ◽  
Erick Ballestero ◽  
Simone Sommer

The skin microbiome is an important part of amphibian immune defenses and protects against pathogens such as the chytrid fungus Batrachochytrium dendrobatidis (Bd), which causes the skin disease chytridiomycosis. Alteration of the microbiome by anthropogenic factors, like pesticides, can impact this protective trait, disrupting its functionality. Chlorothalonil is a widely used fungicide that has been recognized as having an impact on amphibians, but so far, no studies have investigated its effects on amphibian microbial communities. In the present study, we used the amphibian Lithobates vibicarius from the montane forest of Costa Rica, which now appears to persist despite ongoing Bd-exposure, as an experimental model organism. We used 16S rRNA amplicon sequencing to investigate the effect of chlorothalonil on tadpoles’ skin microbiome. We found that exposure to chlorothalonil changes bacterial community composition, with more significant changes at a higher concentration. We also found that a larger number of bacteria were reduced on tadpoles’ skin when exposed to the higher concentration of chlorothalonil. We detected four presumed Bd-inhibitory bacteria being suppressed on tadpoles exposed to the fungicide. Our results suggest that exposure to a widely used fungicide could be impacting host-associated bacterial communities, potentially disrupting an amphibian protective trait against pathogens.


2021 ◽  
Author(s):  
Wesley James Neely ◽  
Sasha E Greenspan ◽  
Leigha M Stahl ◽  
Sam D Heraghty ◽  
Vanessa M Marshall ◽  
...  

Abstract Anthropogenic habitat disturbances can dramatically alter ecological community interactions, including host-pathogen dynamics. Recent work has highlighted the potential for habitat disturbances to alter host-associated microbial communities, but the associations between anthropogenic disturbance, host microbiomes, and pathogens are unresolved. Amphibian skin microbial communities are particularly responsive to factors like temperature, physiochemistry, pathogen infection, and environmental microbial reservoirs. Through a field survey on wild populations of Acris crepitans (Hylidae) and Lithobates catesbeianus (Ranidae), we assessed effects of habitat disturbance on environmental bacterial resevoirs, Batrachochytrium dendrobatidis (Bd) infection, and skin microbiome composition. We found higher measures of microbiome dispersion (a measure of community stability) in A. crepitans from more disturbed ponds, supporting the hypothesis that disturbance increases stochasticity in biological communties. We also found that habitat disturbance limited microbiome similarity between locations for both species, suggesting less bacterial exchange in more disturbed areas. Higher disturbance was associated with lower Bd prevalence for A. crepitans, which could signify suboptimal microclimates for Bd in disturbed habitats. In this system we use microbiome dispersion as a metric of population health. Combined, our findings show that reduced microbiome stability stemming from habitat disturbance could compromise population health, even in the absence of pathogenic infection.


2014 ◽  
Vol 80 (13) ◽  
pp. 4034-4041 ◽  
Author(s):  
Whitney M. Holden ◽  
Alexander R. Ebert ◽  
Peter F. Canning ◽  
Louise A. Rollins-Smith

ABSTRACTChytridiomycosis, an amphibian skin disease caused by the emerging fungal pathogenBatrachochytrium dendrobatidis, has been implicated in catastrophic global amphibian declines. The result is an alarming decrease in amphibian diversity that is a great concern for the scientific community. Clinical trials testing potential antifungal drugs are needed to identify alternative treatments for amphibians infected with this pathogen. In this study, we quantified the MICs of chloramphenicol (800 μg/ml), amphotericin B (0.8 to 1.6 μg/ml), and itraconazole (Sporanox) (20 ng/ml) againstB. dendrobatidis. Both chloramphenicol and amphotericin B significantly reducedB. dendrobatidisinfection in naturally infected southern leopard frogs (Rana[Lithobates]sphenocephala), although neither drug was capable of complete fungal clearance. Long-term exposure ofR. sphenocephalato these drugs did not inhibit antimicrobial peptide (AMP) synthesis, indicating that neither drug is detrimental to this important innate skin defense. However, we observed that chloramphenicol, but not amphotericin B or itraconazole, inhibited the growth of multipleR. sphenocephalaskin bacterial isolatesin vitroat concentrations below the MIC againstB. dendrobatidis. These results indicate that treatment with chloramphenicol might dramatically alter the protective natural skin microbiome when used as an antifungal agent. This study represents the first examination of the effects of alternative antifungal drug treatments on amphibian innate skin defenses, a crucial step to validating these treatments for practical applications.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3688 ◽  
Author(s):  
Myra C. Hughey ◽  
Janelle A. Pena ◽  
Roberto Reyes ◽  
Daniel Medina ◽  
Lisa K. Belden ◽  
...  

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.


2019 ◽  
Vol 6 (9) ◽  
pp. 191080 ◽  
Author(s):  
Carl N. Keiser ◽  
Trina Wantman ◽  
Eria A. Rebollar ◽  
Reid N. Harris

Individual differences in host phenotypes can generate heterogeneity in the acquisition and transmission of microbes. Although this has become a prominent factor of disease epidemiology, host phenotypic variation might similarly underlie the transmission of microbial symbionts that defend against pathogen infection. Here, we test whether host body size and behaviour influence the social acquisition of a skin bacterium, Janthinobacterium lividum , which in some hosts can confer protection against infection by Batrachochytrium dendrobatidis , the causative agent of the amphibian skin disease chytridiomycosis. We measured body size and boldness (time spent in an open field) of green frog tadpoles and haphazardly constructed groups of six individuals. In some groups, we exposed one individual in each group to J. lividum and, in other groups, we inoculated a patch of aquarium pebbles to J. lividum . After 24 h, we swabbed each individual to estimate the presence of J. lividum on their skin. On average, tadpoles acquired nearly four times more bacteria when housed with an exposed individual compared to those housed with a patch of inoculated substrate. When tadpoles were housed with an exposed group-mate, larger and ‘bolder’ individuals acquired more bacteria. These data suggest that phenotypically biased acquisition of defensive symbionts might generate biased patterns of mortality from the pathogens against which they protect.


2019 ◽  
Vol 286 (1896) ◽  
pp. 20182378 ◽  
Author(s):  
Michel E. B. Ohmer ◽  
Rebecca L. Cramp ◽  
Craig R. White ◽  
Peter S. Harlow ◽  
Michael S. McFadden ◽  
...  

Amphibian skin is highly variable in structure and function across anurans, and plays an important role in physiological homeostasis and immune defence. For example, skin sloughing has been shown to reduce pathogen loads on the skin, such as the lethal fungus Batrachochytrium dendrobatidis ( Bd ), but interspecific variation in sloughing frequency is largely unknown. Using phylogenetic linear mixed models, we assessed the relationship between skin turnover rate, skin morphology, ecological traits and overall evidence of Bd -driven declines. We examined skin sloughing rates in 21 frog species from three continents, as well as structural skin characteristics measured from preserved specimens. We found that sloughing rate varies significantly with phylogenetic group, but was not associated with evidence of Bd -driven declines, or other skin characteristics examined. This is the first comparison of sloughing rate across a wide range of amphibian species, and creates the first database of amphibian sloughing behaviour. Given the strong phylogenetic signal observed in sloughing rate, approximate sloughing rates of related species may be predicted based on phylogenetic position. While not related to available evidence of declines, understanding variation in sloughing rate may help explain differences in the severity of infection in genera with relatively slow skin turnover rates (e.g. Atelopus ).


2017 ◽  
Vol 284 (1857) ◽  
pp. 20170944 ◽  
Author(s):  
Andrea J. Jani ◽  
Roland A. Knapp ◽  
Cheryl J. Briggs

Infectious diseases have serious impacts on human and wildlife populations, but the effects of a disease can vary, even among individuals or populations of the same host species. Identifying the reasons for this variation is key to understanding disease dynamics and mitigating infectious disease impacts, but disentangling cause and correlation during natural outbreaks is extremely challenging. This study aims to understand associations between symbiotic bacterial communities and an infectious disease, and examines multiple host populations before or after pathogen invasion to infer likely causal links. The results show that symbiotic bacteria are linked to fundamentally different outcomes of pathogen infection: host–pathogen coexistence (endemic infection) or host population extirpation (epidemic infection). Diversity and composition of skin-associated bacteria differed between populations of the frog, Rana sierrae , that coexist with or were extirpated by the fungal pathogen, Batrachochytrium dendrobatidis (Bd). Data from multiple populations sampled before or after pathogen invasion were used to infer cause and effect in the relationship between the fungal pathogen and symbiotic bacteria. Among host populations, variation in the composition of the skin microbiome was most strongly predicted by pathogen infection severity, even in analyses where the outcome of infection did not vary. This result suggests that pathogen infection shapes variation in the skin microbiome across host populations that coexist with or are driven to extirpation by the pathogen. By contrast, microbiome richness was largely unaffected by pathogen infection intensity, but was strongly predicted by geographical region of the host population, indicating the importance of environmental or host genetic factors in shaping microbiome richness. Thus, while both richness and composition of the microbiome differed between endemic and epidemic host populations, the underlying causes are most likely different: pathogen infection appears to shape microbiome composition, while microbiome richness was less sensitive to pathogen-induced disturbance. Because higher richness was correlated with host persistence in the presence of Bd, and richness appeared relatively stable to Bd infection, microbiome richness may contribute to disease resistance, although the latter remains to be directly tested.


PLoS ONE ◽  
2013 ◽  
Vol 8 (3) ◽  
pp. e59499 ◽  
Author(s):  
Ana V. Longo ◽  
David Rodriguez ◽  
Domingos da Silva Leite ◽  
Luís Felipe Toledo ◽  
Cinthya Mendoza Almeralla ◽  
...  

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