Molecular chaperone accumulation as a function of stress evidences adaptation to high hydrostatic pressure in the piezophilic archaeon Thermococcus barophilus

Abstract

The accumulation of mannosyl-glycerate (MG), the salinity stress response osmolyte of Thermococcales, was investigated as a function of hydrostatic pressure in Thermococcus barophilus strain MP, a hyperthermophilic, piezophilic archaeon isolated from the Snake Pit site (MAR), which grows optimally at 40 MPa. Strain MP accumulated MG primarily in response to salinity stress, but in contrast to other Thermococcales, MG was also accumulated in response to thermal stress. MG accumulation peaked for combined stresses. The accumulation of MG was drastically increased under sub-optimal hydrostatic pressure conditions, demonstrating that low pressure is perceived as a stress in this piezophile, and that the proteome of T. barophilus is low-pressure sensitive. MG accumulation was strongly reduced under supra-optimal pressure conditions clearly demonstrating the structural adaptation of this proteome to high hydrostatic pressure. The lack of MG synthesis only slightly altered the growth characteristics of two different MG synthesis deletion mutants. No shift to other osmolytes was observed. Altogether our observations suggest that the salinity stress response in T. barophilus is not essential and may be under negative selective pressure, similarly to what has been observed for its thermal stress response.

Figure 1

MG synthesis pathway (A, adapted from ref. 20) and genetic organization (B).

Figure 2. MG accumulation in T. barophilus as a function of pressure, in response to salt and temperature stress.

Thermal stress conditions under optimal salinity (3% NaCl) and pressure (40 MPa) conditions for growth are highlighted by a red rectangle. Salinity stress conditions under optimal temperature (85 °C) and pressure (40 MPa) are highlighted by a green rectangle. NG (No growth) P/T/salinity combination incompatible with growth of T. barophilus, e.g. 98 °C at atmospheric pressure. NA: Not analyzed.