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Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans

Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal), using...

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Autores principales: Carter, Edward Davis, Bletz, Molly C., Le Sage, Mitchell, LaBumbard, Brandon, Rollins-Smith, Louise A., Woodhams, Douglas C., Miller, Debra L., Gray, Matthew J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7891748/
https://www.ncbi.nlm.nih.gov/pubmed/33600433
http://dx.doi.org/10.1371/journal.ppat.1009234
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author Carter, Edward Davis
Bletz, Molly C.
Le Sage, Mitchell
LaBumbard, Brandon
Rollins-Smith, Louise A.
Woodhams, Douglas C.
Miller, Debra L.
Gray, Matthew J.
author_facet Carter, Edward Davis
Bletz, Molly C.
Le Sage, Mitchell
LaBumbard, Brandon
Rollins-Smith, Louise A.
Woodhams, Douglas C.
Miller, Debra L.
Gray, Matthew J.
author_sort Carter, Edward Davis
collection PubMed
description Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal), using controlled laboratory experiments, and measured components of host immune defense to identify regulating mechanisms. We found that adult and juvenile Notophthalmus viridescens died faster due to Bsal chytridiomycosis at 14°C than at 6 and 22°C. Pathogen replication rates, total available proteins on the skin, and microbiome composition likely drove these relationships. Temperature-dependent skin microbiome composition in our laboratory experiments matched seasonal trends in wild N. viridescens, adding validity to these results. We also found that hydrophobic peptide production after two months post-exposure to Bsal was reduced in infected animals compared to controls, perhaps due to peptide release earlier in infection or impaired granular gland function in diseased animals. Using our temperature-dependent susceptibility results, we performed a geographic analysis that revealed N. viridescens populations in the northeastern United States and southeastern Canada are at greatest risk for Bsal invasion, which shifted risk north compared to previous assessments. Our results indicate that environmental temperature will play a key role in the epidemiology of Bsal and provide evidence that temperature manipulations may be a viable disease management strategy.
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spelling pubmed-78917482021-03-01 Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans Carter, Edward Davis Bletz, Molly C. Le Sage, Mitchell LaBumbard, Brandon Rollins-Smith, Louise A. Woodhams, Douglas C. Miller, Debra L. Gray, Matthew J. PLoS Pathog Research Article Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans (Bsal), using controlled laboratory experiments, and measured components of host immune defense to identify regulating mechanisms. We found that adult and juvenile Notophthalmus viridescens died faster due to Bsal chytridiomycosis at 14°C than at 6 and 22°C. Pathogen replication rates, total available proteins on the skin, and microbiome composition likely drove these relationships. Temperature-dependent skin microbiome composition in our laboratory experiments matched seasonal trends in wild N. viridescens, adding validity to these results. We also found that hydrophobic peptide production after two months post-exposure to Bsal was reduced in infected animals compared to controls, perhaps due to peptide release earlier in infection or impaired granular gland function in diseased animals. Using our temperature-dependent susceptibility results, we performed a geographic analysis that revealed N. viridescens populations in the northeastern United States and southeastern Canada are at greatest risk for Bsal invasion, which shifted risk north compared to previous assessments. Our results indicate that environmental temperature will play a key role in the epidemiology of Bsal and provide evidence that temperature manipulations may be a viable disease management strategy. Public Library of Science 2021-02-18 /pmc/articles/PMC7891748/ /pubmed/33600433 http://dx.doi.org/10.1371/journal.ppat.1009234 Text en © 2021 Carter et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Carter, Edward Davis
Bletz, Molly C.
Le Sage, Mitchell
LaBumbard, Brandon
Rollins-Smith, Louise A.
Woodhams, Douglas C.
Miller, Debra L.
Gray, Matthew J.
Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans
title Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans
title_full Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans
title_fullStr Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans
title_full_unstemmed Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans
title_short Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans
title_sort winter is coming–temperature affects immune defenses and susceptibility to batrachochytrium salamandrivorans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7891748/
https://www.ncbi.nlm.nih.gov/pubmed/33600433
http://dx.doi.org/10.1371/journal.ppat.1009234
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