Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia

ABSTRACT The majority of fungal species prefer the 12° to 30°C range, and relatively few species tolerate temperatures higher than 35°C. Our understanding of the mechanisms underpinning the ability of some species to grow at higher temperatures is incomplete. Nosema ceranae is an obligate intracellu...

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Autores principales:	Nora K. McNamara-Bordewick, Mia McKinstry, Jonathan W. Snow
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	heat shock factor honey bee Nosema heat shock response microsporidia proteostasis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/dd9fd65a37fa411cb45c650094ac0e64
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spelling	oai:doaj.org-article:dd9fd65a37fa411cb45c650094ac0e642021-11-15T15:22:20ZRobust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia10.1128/mSphere.00219-192379-5042https://doaj.org/article/dd9fd65a37fa411cb45c650094ac0e642019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00219-19https://doaj.org/toc/2379-5042ABSTRACT The majority of fungal species prefer the 12° to 30°C range, and relatively few species tolerate temperatures higher than 35°C. Our understanding of the mechanisms underpinning the ability of some species to grow at higher temperatures is incomplete. Nosema ceranae is an obligate intracellular fungal parasite that infects honey bees and can cause individual mortality and contribute to colony collapse. Despite a reduced genome, this species is strikingly thermotolerant, growing optimally at the colony temperature of 35°C. In characterizing the heat shock response (HSR) in N. ceranae, we found that this and other microsporidian species have lost the transcriptional regulator HSF and possess a reduced set of putative core HSF1-dependent HSR target genes. Despite these losses, N. ceranae demonstrates robust upregulation of the remaining HSR target genes after heat shock. In addition, thermal stress leads to alterations in genes involved in various metabolic pathways, ribosome biogenesis and translation, and DNA repair. These results provide important insight into the stress responses of microsporidia. Such a new understanding will allow new comparisons with other pathogenic fungi and potentially enable the discovery of novel treatment strategies for microsporidian infections affecting food production and human health. IMPORTANCE We do not fully understand why some fungal species are able to grow at temperatures approaching mammalian body temperature. Nosema ceranae, a microsporidium, is a type of fungal parasite that infects honey bees and grows optimally at the colony temperature of 35°C despite possessing cellular machinery for responding to heat stress that is notably simpler than that of other fungi. We find that N. ceranae demonstrates a robust and broad response to heat shock. These results provide important insight into the stress responses of this type of fungus, allow new comparisons with other pathogenic fungi, and potentially enable the discovery of novel treatment strategies for this type of fungus.Nora K. McNamara-BordewickMia McKinstryJonathan W. SnowAmerican Society for Microbiologyarticleheat shock factorhoney beeNosemaheat shock responsemicrosporidiaproteostasisMicrobiologyQR1-502ENmSphere, Vol 4, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	heat shock factor honey bee Nosema heat shock response microsporidia proteostasis Microbiology QR1-502
spellingShingle	heat shock factor honey bee Nosema heat shock response microsporidia proteostasis Microbiology QR1-502 Nora K. McNamara-Bordewick Mia McKinstry Jonathan W. Snow Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia
description	ABSTRACT The majority of fungal species prefer the 12° to 30°C range, and relatively few species tolerate temperatures higher than 35°C. Our understanding of the mechanisms underpinning the ability of some species to grow at higher temperatures is incomplete. Nosema ceranae is an obligate intracellular fungal parasite that infects honey bees and can cause individual mortality and contribute to colony collapse. Despite a reduced genome, this species is strikingly thermotolerant, growing optimally at the colony temperature of 35°C. In characterizing the heat shock response (HSR) in N. ceranae, we found that this and other microsporidian species have lost the transcriptional regulator HSF and possess a reduced set of putative core HSF1-dependent HSR target genes. Despite these losses, N. ceranae demonstrates robust upregulation of the remaining HSR target genes after heat shock. In addition, thermal stress leads to alterations in genes involved in various metabolic pathways, ribosome biogenesis and translation, and DNA repair. These results provide important insight into the stress responses of microsporidia. Such a new understanding will allow new comparisons with other pathogenic fungi and potentially enable the discovery of novel treatment strategies for microsporidian infections affecting food production and human health. IMPORTANCE We do not fully understand why some fungal species are able to grow at temperatures approaching mammalian body temperature. Nosema ceranae, a microsporidium, is a type of fungal parasite that infects honey bees and grows optimally at the colony temperature of 35°C despite possessing cellular machinery for responding to heat stress that is notably simpler than that of other fungi. We find that N. ceranae demonstrates a robust and broad response to heat shock. These results provide important insight into the stress responses of this type of fungus, allow new comparisons with other pathogenic fungi, and potentially enable the discovery of novel treatment strategies for this type of fungus.
format	article
author	Nora K. McNamara-Bordewick Mia McKinstry Jonathan W. Snow
author_facet	Nora K. McNamara-Bordewick Mia McKinstry Jonathan W. Snow
author_sort	Nora K. McNamara-Bordewick
title	Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia
title_short	Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia
title_full	Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia
title_fullStr	Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia
title_full_unstemmed	Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia
title_sort	robust transcriptional response to heat shock impacting diverse cellular processes despite lack of heat shock factor in microsporidia
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/dd9fd65a37fa411cb45c650094ac0e64
work_keys_str_mv	AT norakmcnamarabordewick robusttranscriptionalresponsetoheatshockimpactingdiversecellularprocessesdespitelackofheatshockfactorinmicrosporidia AT miamckinstry robusttranscriptionalresponsetoheatshockimpactingdiversecellularprocessesdespitelackofheatshockfactorinmicrosporidia AT jonathanwsnow robusttranscriptionalresponsetoheatshockimpactingdiversecellularprocessesdespitelackofheatshockfactorinmicrosporidia
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Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in Microsporidia

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