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Novel antimicrobial peptides and peptide-microbiome crosstalk in Appalachian salamander skin

ABSTRACT: Host antimicrobial peptides (AMPs) are an ancient defense system found in all multicellular organisms that interact with host microbiomes. We used multi-omics and mathematical tools to discover new AMPs and examine AMP-microbial interactions in three Appalachian salamander species (Plethodon cinereus, Eurycea bislineata and Notophthalmus viridescens). We conducted skin transcriptomics (n = 13), proteomics (n = 91) and AMP database querying to identify candidate AMPs. With candidate AMPs, we identified correlations with the skin microbiome (16S rRNA amplicon) and synthesized 20 peptides to use in challenge assays with pathogens of amphibians (Batrachochytrium dendrobatidis: Bd) and humans (ESKAPEE pathogen panel). Using transcriptomics, candidate AMP genes (30-67 genes) were detected in all individuals with Cathelidicin-like peptides being most common. Using proteomics, detectable AMPs were only found in a subset of salamanders (31/91) - predominately E. bislineata - with Kinin-like peptides being most common. Candidate AMP composition generally predicted skin bacterial composition. Crude and synthesized peptides showed limited activity against Bd. Two synthesized Cathelicidin-like peptides (from P. cinereus) showed moderate to strong killing activity against human pathogens, Acinetobacter baumannii and Escherichia coli. We show that mining under-studied taxa and using multi-omics fuels AMPs discovery, reveals dynamic AMPs-microbial relationships, and informs the therapeutic potential of AMPs usage in conservation and translational applications.

INSTRUMENT(S): LTQ Orbitrap Elite

ORGANISM(S): Plethodon Cinereus (ncbitaxon:141976) Notophthalmus Viridescens (ncbitaxon:8316) Eurycea Bislineata (ncbitaxon:134758)

SUBMITTER: Carly Muletz-Wolz Timothy Cleland

PROVIDER: MSV000097047 | MassIVE | Wed Feb 05 04:51:00 GMT 2025

SECONDARY ACCESSION(S): PXD060511

REPOSITORIES: MassIVE

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Project description:Emerging infectious diseases are of great concern for both wildlife and humans. Several highly virulent fungal pathogens have recently been discovered in natural populations, highlighting the need for a better understanding of fungal-vertebrate host-pathogen interactions. Because most fungal pathogens are not fatal in the absence of other predisposing conditions, host-pathogen dynamics for deadly fungal pathogens are of particular interest. The chytrid fungus Batrachochytrium dendrobatidis (hereafter Bd) infects hundreds of species of frogs in the wild. It is found worldwide and is a significant contributor to the current global amphibian decline. However, the mechanism by which Bd causes death in amphibians, and the response of the host to Bd infection, remain largely unknown. Here we use whole-genome microarrays to monitor the transcriptional responses to Bd infection in the model frog species, Silurana (Xenopus) tropicalis, which is susceptible to chytridiomycosis. To elucidate the immune response to Bd and evaluate the physiological effects of chytridiomycosis, we measured gene expression changes in several tissues (liver, skin, spleen) following exposure to Bd. We detected a strong transcriptional response for genes involved in physiological processes that can help explain some clinical symptoms of chytridiomycosis at the organismal level. However, we detected surprisingly little evidence of an immune response to Bd exposure, suggesting that this susceptible species may not be mounting efficient innate and adaptive immune responses against Bd. The weak immune response may be partially explained by the thermal conditions of the experiment, which were optimal for Bd growth. However, many immune genes exhibited decreased expression in Bd-exposed frogs compared to control frogs, suggesting a more complex effect of Bd on the immune system than simple temperature-mediated immune suppression. This study generates important baseline data for ongoing efforts to understand differences in response to Bd between susceptible and resistant frog species and the effects of chytridiomycosis in natural populations.

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Novel antimicrobial peptides and peptide-microbiome crosstalk in Appalachian salamander skin

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