Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.

Amphibians are experiencing a panzootic of unprecedented proportions caused by the emergence of Batrachochytrium dendrobatidis (Bd). However, all species are not equally at risk of infection, and risk is further modified by environmental variables, specifically temperature. In order to understand ho...

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Main Authors: Laia Ribas, Ming-Shi Li, Benjamin J Doddington, Jacques Robert, Judith A Seidel, J Simon Kroll, Lyle B Zimmerman, Nicholas C Grassly, Trenton W J Garner, Matthew C Fisher
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-12-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2794374?pdf=render
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spelling doaj-ed934a09e94246b99af3cd27f8421c852020-11-24T21:41:58ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-12-01412e840810.1371/journal.pone.0008408Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.Laia RibasMing-Shi LiBenjamin J DoddingtonJacques RobertJudith A SeidelJ Simon KrollLyle B ZimmermanNicholas C GrasslyTrenton W J GarnerMatthew C FisherAmphibians are experiencing a panzootic of unprecedented proportions caused by the emergence of Batrachochytrium dendrobatidis (Bd). However, all species are not equally at risk of infection, and risk is further modified by environmental variables, specifically temperature. In order to understand how, and when, hosts mount a response to Bd we analysed infection dynamics and patterns of gene expression in the model amphibian species Silurana (Xenopus) tropicalis. Mathematical modelling of infection dynamics demonstrate the existence of a temperature-dependent protective response that is largely independent of the intrinsic growth-rate of Bd. Using temporal expression-profiling by microarrays and qRT-PCR, we characterise this response in the main amphibian lymphoid tissue, the spleen. We demonstrate that clearance of Bd at the host-optimal temperature is not clearly associated with an adaptive immune response, but rather is correlated with the induction of components of host innate immunity including the expression of genes that are associated with the production of the antimicrobial skin peptide preprocareulein (PPCP) as well as inflammatory responses. We find that adaptive immunity appears to be lacking at host-optimal temperatures. This suggests that either Bd does not stimulate, or suppresses, adaptive immunity, or that trade-offs exist between innate and adaptive limbs of the amphibian immune system. At cold temperatures, S. tropicalis loses the ability to mount a PPCP-based innate response, and instead manifests a more pronounced inflammatory reaction that is characterised by the production of proteases and higher pathogen burdens. This study demonstrates the temperature-dependency of the amphibian response to infection by Bd and indicates the influence that changing climates may exert on the ectothermic host response to pathogens.http://europepmc.org/articles/PMC2794374?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Laia Ribas
Ming-Shi Li
Benjamin J Doddington
Jacques Robert
Judith A Seidel
J Simon Kroll
Lyle B Zimmerman
Nicholas C Grassly
Trenton W J Garner
Matthew C Fisher
spellingShingle Laia Ribas
Ming-Shi Li
Benjamin J Doddington
Jacques Robert
Judith A Seidel
J Simon Kroll
Lyle B Zimmerman
Nicholas C Grassly
Trenton W J Garner
Matthew C Fisher
Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.
PLoS ONE
author_facet Laia Ribas
Ming-Shi Li
Benjamin J Doddington
Jacques Robert
Judith A Seidel
J Simon Kroll
Lyle B Zimmerman
Nicholas C Grassly
Trenton W J Garner
Matthew C Fisher
author_sort Laia Ribas
title Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.
title_short Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.
title_full Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.
title_fullStr Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.
title_full_unstemmed Expression profiling the temperature-dependent amphibian response to infection by Batrachochytrium dendrobatidis.
title_sort expression profiling the temperature-dependent amphibian response to infection by batrachochytrium dendrobatidis.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2009-12-01
description Amphibians are experiencing a panzootic of unprecedented proportions caused by the emergence of Batrachochytrium dendrobatidis (Bd). However, all species are not equally at risk of infection, and risk is further modified by environmental variables, specifically temperature. In order to understand how, and when, hosts mount a response to Bd we analysed infection dynamics and patterns of gene expression in the model amphibian species Silurana (Xenopus) tropicalis. Mathematical modelling of infection dynamics demonstrate the existence of a temperature-dependent protective response that is largely independent of the intrinsic growth-rate of Bd. Using temporal expression-profiling by microarrays and qRT-PCR, we characterise this response in the main amphibian lymphoid tissue, the spleen. We demonstrate that clearance of Bd at the host-optimal temperature is not clearly associated with an adaptive immune response, but rather is correlated with the induction of components of host innate immunity including the expression of genes that are associated with the production of the antimicrobial skin peptide preprocareulein (PPCP) as well as inflammatory responses. We find that adaptive immunity appears to be lacking at host-optimal temperatures. This suggests that either Bd does not stimulate, or suppresses, adaptive immunity, or that trade-offs exist between innate and adaptive limbs of the amphibian immune system. At cold temperatures, S. tropicalis loses the ability to mount a PPCP-based innate response, and instead manifests a more pronounced inflammatory reaction that is characterised by the production of proteases and higher pathogen burdens. This study demonstrates the temperature-dependency of the amphibian response to infection by Bd and indicates the influence that changing climates may exert on the ectothermic host response to pathogens.
url http://europepmc.org/articles/PMC2794374?pdf=render
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