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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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Effects of temperature on the interaction between amphibian skin bacteria and Batrachochytrium dendrobatidis
Symbiotic relationships between animals and microbes are important for a range of functions, from digestion to protection from pathogens. However, the impact of temperature variation on these animal-microbe interactions remains poorly understood. Amphibians have experienced population declines and even extinctions on a global scale due to chytridiomycosis, a disease caused by chytrid fungi in the genusBatrachochytrium. Variation in susceptibility to this disease exists within and among host species. While the mechanisms generating differences in host susceptibility remain elusive, differences in immune system components, as well as variation in host and environmental temperatures, have been associated with this variation. The symbiotic cutaneous bacteria of amphibians are another potential cause for variation in susceptibility to chytridiomycosis, with some bacterial species producing antifungal metabolites that prevent the growth ofBd. The growth of bothBdand bacteria are affected by temperature, and thus we hypothesized that amphibian skin bacteria may be more effective at preventingBdgrowth at certain temperatures. To test this, we collected bacteria from the skins of frogs, harvested the metabolites they produced when grown at three different temperatures, and then grewBdin the presence of those metabolites under those same three temperatures in a three-by-three fully crossed design. We found that both the temperature at which cutaneous bacteria were grown (and metabolites produced) as well as the temperature at whichBdis grown can impact the ability of cutaneous bacteria to inhibit the growth ofBd. While some bacterial isolates showed the ability to inhibitBdgrowth across multiple temperature treatments, no isolate was found to be inhibitive across all combinations of bacterial incubation orBdchallenge temperatures, suggesting that temperature affects both the metabolites produced and the effectiveness of those metabolites against theBdpathogen. These findings move us closer to a mechanistic understanding of why chytridiomycosis outbreaks and related amphibian declines are often limited to certain climates and seasons.
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- Award ID(s):
- 2120084
- PAR ID:
- 10512693
- Publisher / Repository:
- Frontiers in Microbiology
- Date Published:
- Journal Name:
- Frontiers in Microbiology
- Volume:
- 14
- ISSN:
- 1664-302X
- 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/fmicb.2023.1253482
