Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt species
A diverse metabolome exists on amphibian skin that mediates interactions between hosts and skin microbiomes. Tetrodotoxin is one such metabolite that occurs across a variety of taxa, and is particularly well studied in newts of the genus Taricha that are susceptible to infection with chytrid fungi....
Saved in:
Main Authors: | , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2025-01-01
|
Series: | Frontiers in Amphibian and Reptile Science |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/famrs.2024.1503056/full |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1832583706009665536 |
---|---|
author | Talon Jost Talon Jost Alysha Henderson Brandon LaBumbard Krisztian Magori Amber Stokes Danica Bergin Autumn Holley Autumn Holley Molly Bletz Molly Bletz Obed Hernández-Gómez Gary Bucciarelli Douglas C. Woodhams Jonah Piovia-Scott Jenifer B. Walke |
author_facet | Talon Jost Talon Jost Alysha Henderson Brandon LaBumbard Krisztian Magori Amber Stokes Danica Bergin Autumn Holley Autumn Holley Molly Bletz Molly Bletz Obed Hernández-Gómez Gary Bucciarelli Douglas C. Woodhams Jonah Piovia-Scott Jenifer B. Walke |
author_sort | Talon Jost |
collection | DOAJ |
description | A diverse metabolome exists on amphibian skin that mediates interactions between hosts and skin microbiomes. Tetrodotoxin is one such metabolite that occurs across a variety of taxa, and is particularly well studied in newts of the genus Taricha that are susceptible to infection with chytrid fungi. The interaction of tetrodotoxin with the skin microbiome, including pathogenic fungi, is not well understood, and here we describe these patterns across 12 populations of Taricha granulosa and T. torosa in Washington, Oregon, and California. We found no correlation of TTX and Batrachochytrium dendrobatidis (Bd) infection in either T. granulosa or T. torosa, a pattern inconsistent with a previous study. In addition, TTX, but not Bd, was significantly correlated with the skin microbiome composition in T. granulosa. In T. torosa, however, Bd, but not TTX, was correlated with the skin microbiome structure. The relationship between TTX and skin microbiome composition differed between species, with significant correlations observed only in T. granulosa, which exhibited higher TTX concentrations. We also detected significantly higher abundances of bacterial taxa (e.g., Pseudomonadaceae) associated with TTX production in newts with higher skin TTX. These taxa (ASVs matching Aeromonas, Pseudomonas, Shewanella, and Sphingopyxis) were associated with all body sites of previously sampled T. granulosa, but not found in soil samples. Our results suggest that toxins can shape the newt skin microbiome and may influence pathogen infection through indirect mechanisms, as TTX showed no direct inhibition of Bd or B. salamandrivorans growth. |
format | Article |
id | doaj-art-2edbf60696b6451a940d82469410d7e7 |
institution | Kabale University |
issn | 2813-6780 |
language | English |
publishDate | 2025-01-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Amphibian and Reptile Science |
spelling | doaj-art-2edbf60696b6451a940d82469410d7e72025-01-28T06:41:21ZengFrontiers Media S.A.Frontiers in Amphibian and Reptile Science2813-67802025-01-01210.3389/famrs.2024.15030561503056Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt speciesTalon Jost0Talon Jost1Alysha Henderson2Brandon LaBumbard3Krisztian Magori4Amber Stokes5Danica Bergin6Autumn Holley7Autumn Holley8Molly Bletz9Molly Bletz10Obed Hernández-Gómez11Gary Bucciarelli12Douglas C. Woodhams13Jonah Piovia-Scott14Jenifer B. Walke15Department of Biology, Eastern Washington University, Cheney, WA, United StatesDepartment of Ecosystem Science and Management, Pennsylvania State University, State College, PA, United StatesSchool of Biological Sciences, Washington State University, Vancouver, WA, United StatesDepartment of Biology, University of Massachusetts Boston, Boston, MA, United StatesDepartment of Biology, Eastern Washington University, Cheney, WA, United StatesDepartment of Biology, California State University Bakersfield, Bakersfield, CA, United StatesDepartment of Biology, California State University Bakersfield, Bakersfield, CA, United StatesDepartment of Biology, Eastern Washington University, Cheney, WA, United StatesSchool of Natural Resources, University of Tennessee Knoxville, Knoxville, TN, United StatesDepartment of Ecosystem Science and Management, Pennsylvania State University, State College, PA, United StatesDepartment of Biology, University of Massachusetts Boston, Boston, MA, United StatesDepartment of Fish, Wildlife and Conservation Ecology, New Mexico State University, Las Cruces, NM, United StatesDepartment of Natural Resources, University of California, Davis, Davis, CA, United StatesDepartment of Biology, University of Massachusetts Boston, Boston, MA, United StatesSchool of Biological Sciences, Washington State University, Vancouver, WA, United StatesDepartment of Biology, Eastern Washington University, Cheney, WA, United StatesA diverse metabolome exists on amphibian skin that mediates interactions between hosts and skin microbiomes. Tetrodotoxin is one such metabolite that occurs across a variety of taxa, and is particularly well studied in newts of the genus Taricha that are susceptible to infection with chytrid fungi. The interaction of tetrodotoxin with the skin microbiome, including pathogenic fungi, is not well understood, and here we describe these patterns across 12 populations of Taricha granulosa and T. torosa in Washington, Oregon, and California. We found no correlation of TTX and Batrachochytrium dendrobatidis (Bd) infection in either T. granulosa or T. torosa, a pattern inconsistent with a previous study. In addition, TTX, but not Bd, was significantly correlated with the skin microbiome composition in T. granulosa. In T. torosa, however, Bd, but not TTX, was correlated with the skin microbiome structure. The relationship between TTX and skin microbiome composition differed between species, with significant correlations observed only in T. granulosa, which exhibited higher TTX concentrations. We also detected significantly higher abundances of bacterial taxa (e.g., Pseudomonadaceae) associated with TTX production in newts with higher skin TTX. These taxa (ASVs matching Aeromonas, Pseudomonas, Shewanella, and Sphingopyxis) were associated with all body sites of previously sampled T. granulosa, but not found in soil samples. Our results suggest that toxins can shape the newt skin microbiome and may influence pathogen infection through indirect mechanisms, as TTX showed no direct inhibition of Bd or B. salamandrivorans growth.https://www.frontiersin.org/articles/10.3389/famrs.2024.1503056/fullBatrachochytrium dendrobatidisBatrachochytrium salamandrivoranschytridiomycosisdisease ecologymicrobial ecologyTTX |
spellingShingle | Talon Jost Talon Jost Alysha Henderson Brandon LaBumbard Krisztian Magori Amber Stokes Danica Bergin Autumn Holley Autumn Holley Molly Bletz Molly Bletz Obed Hernández-Gómez Gary Bucciarelli Douglas C. Woodhams Jonah Piovia-Scott Jenifer B. Walke Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt species Frontiers in Amphibian and Reptile Science Batrachochytrium dendrobatidis Batrachochytrium salamandrivorans chytridiomycosis disease ecology microbial ecology TTX |
title | Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt species |
title_full | Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt species |
title_fullStr | Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt species |
title_full_unstemmed | Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt species |
title_short | Tetrodotoxin, fungal pathogen infection, and bacterial microbiome associations are variable in the skin microecosystems of two Taricha newt species |
title_sort | tetrodotoxin fungal pathogen infection and bacterial microbiome associations are variable in the skin microecosystems of two taricha newt species |
topic | Batrachochytrium dendrobatidis Batrachochytrium salamandrivorans chytridiomycosis disease ecology microbial ecology TTX |
url | https://www.frontiersin.org/articles/10.3389/famrs.2024.1503056/full |
work_keys_str_mv | AT talonjost tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT talonjost tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT alyshahenderson tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT brandonlabumbard tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT krisztianmagori tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT amberstokes tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT danicabergin tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT autumnholley tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT autumnholley tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT mollybletz tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT mollybletz tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT obedhernandezgomez tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT garybucciarelli tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT douglascwoodhams tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT jonahpioviascott tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies AT jeniferbwalke tetrodotoxinfungalpathogeninfectionandbacterialmicrobiomeassociationsarevariableintheskinmicroecosystemsoftwotarichanewtspecies |