The thermoacidophilic archaeon Sulfolobus acidocaldarius employs diverse strategies to thrive in extreme environments. At the cellular level, stress responses include increased motility and DNA uptake upon UV irradiation 1, enhanced biofilm formation under organic solvent exposure 2, and specific responses to nutrient starvation 3, showcasing its adaptability to various challenges.
At the molecular level, trehalose and polyphosphate (polyP) metabolism play critical roles in stress resilience. Trehalose acts as a compatible solute stabilizing macromolecules and membranes, synthesized via three distinct pathways 4. A triple mutant lacking all pathways failed to grow under salt stress, while wild-type cells showed increased trehalose levels under salt stress, emphasizing its role in osmotic stress protection.
PolyP functions as an energy and phosphate reserve, contributing to homeostasis under stress. We identified a novel archaeal polyphosphate kinase, SaPPK3, with reversible activity that drives ATP formation under low energy charge 5. With a combined experimental modelling approach using quantitative 31P NMR, we demonstrated that SaPPK3 buffers energy under stress, synthesizing polyP only when ATP/ADP ratios are high. Phylogenetic analyses place SaPPK3 in a new PPK3 family, patchily distributed across Archaea and Bacteria.
Together, these findings provide a deeper understanding of the molecular strategies employed by S. acidocaldarius to cope with extreme conditions, contributing to our broader knowledge of archaeal stress physiology and offering potential applications in biotechnology and industrial microbiology.
1 Schult, F. et al. Nucleic Acids Res (2018). https://doi.org/10.1093/nar/gky527
2 Benninghoff, J. C. et al. Applied and environmental microbiology 87 (2021). https://doi.org/10.1128/aem.02988-20
3 Bischof, L. F. et al. Frontiers in microbiology 9, 3201 (2018). https://doi.org/10.3389/fmicb.2018.03201
4 Stracke, C. et al. Applied and environmental microbiology 86 (2020). https://doi.org/10.1128/aem.01565-20
5 Höfmann, S. et al. bioRxiv (2024). https://doi.org/10.1101/2024.08.28.610084