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.
Highlights
Fungal species are highly varied in their tolerance to high temperature, the majority prefer the range of 12° to 30°C, and relatively few species tolerate temperatures higher than 35°C [1]
We found that some of the most highly induced genes after heat shock are involved in carbon and nitrogen metabolism
We observed that thermal stress leads to alterations in many genes involved in other cellular processes, such as ribosome biogenesis and translation, DNA repair, and redox status (Table S3)
Summary
Fungal species are highly varied in their tolerance to high temperature, the majority prefer the range of 12° to 30°C, and relatively few species tolerate temperatures higher than 35°C [1]. Comparative genomics indicates that N. ceranae, and microsporidia more broadly, have lost many of the cellular processes and pathways found in free-living eukaryotes [13]. Despite this genome compaction, N. ceranae exhibits a striking ability to grow at the high temperatures (34 to 35°C) maintained in honey bee colonies [14, 15]. Heat shock induces a significant number of genes encoding proteins of unknown function These results provide an important new understanding of microsporidian cell biology and shed new light on how stress responses in these species compare to other pathogenic fungi. The application of such discoveries to the treatment of microsporidian infections could have important impacts on food production and human health
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