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Host-associated microbiomes play important roles in host health and pathogen defense. In amphibians, the skin-associated microbiota can contribute to innate immunity with potential implications for disease management. Few studies have examined season-long temporal variation in the amphibian skin-associated microbiome, and the interactions between bacteria and fungi on amphibian skin remain poorly understood. We characterize season-long temporal variation in the skin-associated microbiome of the western tiger salamander ( Ambystoma mavortium ) for both bacteria and fungi between sites and across salamander life stages. Two hundred seven skin-associated microbiome samples were collected from salamanders at two Rocky Mountain lakes throughout the summer and fall of 2018, and 127 additional microbiome samples were collected from lake water and lake substrate. We used 16S rRNA and ITS amplicon sequencing with Bayesian Dirichlet-multinomial regression to estimate the relative abundances of bacterial and fungal taxa, test for differential abundance, examine microbial selection, and derive alpha diversity. We predicted the ability of bacterial communities to inhibit the amphibian chytrid fungus Batrachochytrium dendrobatidis ( Bd ), a cutaneous fungal pathogen, using stochastic character mapping and a database of Bd -inhibitory bacterial isolates. For both bacteria and fungi, we observed variation in community composition through time, between sites, and with salamander age and life stage. We further found that temporal trends in community composition were specific to each combination of salamander age, life stage, and lake. We found salamander skin to be selective for microbes, with many taxa disproportionately represented relative to the environment. Salamander skin appeared to select for predicted Bd -inhibitory bacteria, and we found a negative relationship between the relative abundances of predicted Bd -inhibitory bacteria and Bd . We hope these findings will assist in the conservation of amphibian species threatened by chytridiomycosis and other emerging diseases.
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Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders
The emerging fungal pathogen, Batrachochytrium dendrobatidis ( Bd ), which can cause a fatal disease called chytridiomycosis, is implicated in the collapse of hundreds of host amphibian species. We describe chytridiomycosis dynamics in two co-occurring terrestrial salamander species, the Santa Lucia Mountains slender salamander, Batrachoseps luciae , and the arboreal salamander, Aneides lugubris . We (1) conduct a retrospective Bd -infection survey of specimens collected over the last century, (2) estimate present-day Bd infections in wild populations, (3) use generalized linear models (GLM) to identify biotic and abiotic correlates of infection risk, (4) investigate susceptibility of hosts exposed to Bd in laboratory trials, and (5) examine the ability of host skin bacteria to inhibit Bd in culture. Our historical survey of 2,866 specimens revealed that for most of the early 20th century (~1920–1969), Bd was not detected in either species. By the 1990s the proportion of infected specimens was 29 and 17% ( B. luciae and A. lugubris , respectively), and in the 2010s it was 10 and 17%. This was similar to the number of infected samples from contemporary populations (2014–2015) at 10 and 18%. We found that both hosts experience signs of chytridiomycosis and suffered high Bd -caused mortality (88 and 71% for B. luciae and A. lugubris , respectively). Our GLM revealed that Bd -infection probability was positively correlated with intraspecific group size and proximity to heterospecifics but not to abiotic factors such as precipitation, minimum temperature, maximum temperature, mean temperature, and elevation, or to the size of the hosts. Finally, we found that both host species contain symbiotic skin-bacteria that inhibit growth of Bd in laboratory trials. Our results provide new evidence consistent with other studies showing a relatively recent Bd invasion of amphibian host populations in western North America and suggest that the spread of the pathogen may be enabled both through conspecific and heterospecific host interactions. Our results suggest that wildlife disease studies should assess host-pathogen dynamics that consider the interactions and effects of multiple hosts, as well as the historical context of pathogen invasion, establishment, and epizootic to enzootic transitions to better understand and predict disease dynamics.
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- Award ID(s):
- 1633948
- PAR ID:
- 10317414
- Date Published:
- Journal Name:
- Frontiers in Veterinary Science
- Volume:
- 8
- ISSN:
- 2297-1769
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3389/fvets.2021.742288
