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Synopsis Emerging infectious diseases have been of particular interest as a major threat to global biodiversity. In amphibians, two fungal sister taxa, Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal), along with the viral pathogen ranavirus, have affected global populations. Factors such as host traits, abiotic and biotic environmental conditions, and pathogen prevalence contribute to species-specific disease susceptibility. The eastern United States is home to the Appalachian Mountain system, known as a “hotspot” for salamander biodiversity. Bd and ranavirus are present throughout the Appalachians, and a Bsal emergence could be imminent. Throughout the Appalachians are the spotted salamanders, Ambystoma maculatum, a mostly terrestrial salamander that participates in mass breeding migration to ponds and vernal pools in the late spring. Previous experimental studies have shown that spotted salamanders appear to be resistant to Bd and Bsal infection, but the mechanisms behind Bd defense remain unknown. Spotted salamanders emerging from their overwintering habitats were hypothesized to have potent anti-Bd function expressed in their mucus and in their skin microbiomes, as a countermeasure to annual Bd re-emergence. We used non-invasive sampling at two pools during the spotted salamander annual breeding event to (I) determine pathogen prevalence, (II) quantify the antifungal potential of salamander skin mucus, and (III) characterize the diversity and composition of the salamander skin microbiome and contrast it to that of the corresponding environmental microbiome. We did not detect any Bd, Bsal, or ranavirus in the salamanders. The salamander mucus did not inhibit Bd growth in vitro, and anti-Bd bacteria were at low relative abundance in the microbiome. The salamander microbiome sourced a proportion of bacteria from the environment and appeared to select rare taxa from their respective pools; however, their functional relevance in pathogen defense is unclear. Our results suggest that the spotted salamander mucosal secretions and skin microbiome are not the mechanisms of defense against Bd. Rather, elements not captured by the mucosome (e.g., immune cell gene expression) may confer resistance. This study contributes to the understanding of salamander intraspecies variation in disease susceptibility.
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Invasibility of a North American soil ecosystem to amphibian-killing fungal pathogens
North American salamanders are threatened by intercontinental spread of chytridiomycosis, a deadly disease caused by the fungal pathogenBatrachochytrium salamandrivorans(Bsal). To predict potential dispersal ofBsalspores to salamander habitats, we evaluated the capacity of soil microbial communities to resist invasion. We determined the degree of habitat invasibility using soils from five locations throughout the Great Smoky Mountains National Park, a region with a high abundance of susceptible hosts. Our experimental design consisted of replicate soil microcosms exposed to different propagule pressures of the non-native pathogen,Bsal, and an introduced but endemic pathogen,B. dendrobatidis(Bd). To compare growth and competitive interactions, we used quantitative PCR, live/dead cell viability assays, and full-length 16S rRNA sequencing. We found that soil microcosms with intact bacterial communities inhibited bothBsalandBdgrowth, but inhibitory capacity diminished with increased propagule pressure.Bsalshowed greater persistence thanBd. Linear discriminant analysis (LDA) identified the family Burkolderiaceae as increasing in relative abundance with the decline of both pathogens. Although our findings provide evidence of environmental filtering in soils, such barriers weakened in response to pathogen type and propagule pressure, showing that habitats vary their invasibility based on properties of their local microbial communities.
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- Award ID(s):
- 2011278
- PAR ID:
- 10559524
- Publisher / Repository:
- Proceedings of the Royal Society B
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2021
- ISSN:
- 0962-8452
- 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/10.1098/rspb.2023.2658
