Defining heat shock response for the thermoacidophilic model crenarchaeon Sulfolobus acidocaldarius

Abstract

The crenarchaeon Sulfolobus acidocaldarius, growing optimally at temperatures between 75 and 80 °C, thrives in volcanic hot spring habitats that are typified by large temperature gradients, which impose frequent temperature stresses on the cells. Heat shock response is characterized by an upregulation of heat shock proteins, but similar to most (hyper-)thermophilic archaea, S. acidocaldarius seems to be able to bear supra-optimal temperatures with a restricted repertoire of chaperones. Here, we study the physiological consequences of continuous high-temperature stress and rapid heat shock for S. acidocaldarius. Growth experiments and cell viability assays demonstrate that temperatures of 85 °C and higher result in a decreased growth rate and, when the cells are rapidly subjected to a heat shock, a dynamic increase in mRNA levels of all relevant heat shock proteins and a subset of transcription regulators is observed. When exponentially growing cultures are exposed to a heat shock, the survival tipping point is situated around 90 °C, and the rate of heating determines whether cells are able to cope with this stress or whether the defense mechanism immediately fails, leading to extensive cell death. In conclusion, S. acidocaldarius does not seem to be better equipped to handle sudden supra-optimal temperature stress than mesophilic organisms.

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Abbreviations

BR:

Biological replicate

HS:

Heat shock

HSP:

Heat shock protein

Pfdα:

Prefoldin subunit α

Pfdβ:

Prefoldin subunit β

sHSP:

Small heat shock protein

t d :

Doubling time

TF:

Transcription factor

Thα:

Thermosome subunit α

Thβ:

Thermosome subunit β

Thγ:

Thermosome subunit γ

µ :

Specific growth rate

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Acknowledgements

We are grateful to David Sybers for insightful discussions regarding S. acidocaldarius growth curves. We thank Aquila Biolabs for their assistance in setting up a high-temperature on-line growth measurement system. This research was supported by the Research Council of the Vrije Universiteit Brussel and the Research Foundation Flanders (FWO-Vlaanderen) (PhD fellowship 1134419N to Rani Baes, research grant 1526418N and research project G021118).

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Baes, R., Lemmens, L., Mignon, K. et al. Defining heat shock response for the thermoacidophilic model crenarchaeon Sulfolobus acidocaldarius. Extremophiles 24, 681–692 (2020). https://doi.org/10.1007/s00792-020-01184-y

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Keywords

  • Archaea
  • Sulfolobus
  • Heat shock
  • Transcriptional regulation
  • Thermosome