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...
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2019-06-01
|
| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSphere.00219-19 |
| _version_ | 1818567624463745024 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T06:25:46Z |
| format | Article |
| id | doaj.art-dd9fd65a37fa411cb45c650094ac0e64 |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-12-14T06:25:46Z |
| publishDate | 2019-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-dd9fd65a37fa411cb45c650094ac0e642022-12-21T23:13:41ZengAmerican Society for MicrobiologymSphere2379-50422019-06-014310.1128/mSphere.00219-19Robust Transcriptional Response to Heat Shock Impacting Diverse Cellular Processes despite Lack of Heat Shock Factor in MicrosporidiaNora K. McNamara-Bordewick0Mia McKinstry1Jonathan W. Snow2Biology Department, Barnard College, New York, New York, USABiology Department, Barnard College, New York, New York, USABiology Department, Barnard College, New York, New York, USAABSTRACT 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.https://journals.asm.org/doi/10.1128/mSphere.00219-19heat shock factorhoney beeNosemaheat shock responsemicrosporidiaproteostasis |
| spellingShingle | 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 mSphere heat shock factor honey bee Nosema heat shock response microsporidia proteostasis |
| title | 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_short | 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 |
| topic | heat shock factor honey bee Nosema heat shock response microsporidia proteostasis |
| url | https://journals.asm.org/doi/10.1128/mSphere.00219-19 |
| work_keys_str_mv | AT norakmcnamarabordewick robusttranscriptionalresponsetoheatshockimpactingdiversecellularprocessesdespitelackofheatshockfactorinmicrosporidia AT miamckinstry robusttranscriptionalresponsetoheatshockimpactingdiversecellularprocessesdespitelackofheatshockfactorinmicrosporidia AT jonathanwsnow robusttranscriptionalresponsetoheatshockimpactingdiversecellularprocessesdespitelackofheatshockfactorinmicrosporidia |