Loss of the DnaK-DnaJ-GrpE chaperone system among the Aquificales

The DnaK-DnaJ-GrpE (KJE) chaperone system functions at the fulcrum of protein homeostasis in bacteria. It interacts both with nascent polypeptides and with proteins that have become unfolded, either funneling its clients toward the native state or ushering misfolded proteins into degradation. In line with its key role in protein folding, KJE has been considered an essential building block for a minimal bacterial genome and common to all bacteria. In this study, I present a rigorous survey of 1,233 bacterial genomes, which reveals that the entire KJE system is uniquely absent from two members of the order Aquificales, Desulfurobacterium thermolithotrophum, and Thermovibrio ammonificans. The absence of KJE from these free-living bacteria is surprising, particularly in light of the finding that individual losses of grpE and dnaJ are restricted to obligate endosymbionts with highly reduced genomes, whereas dnaK has never been lost in isolation. Examining protein features diagnostic of DnaK substrates in Escherichia coli, radical changes in protein solubility emerge as a likely precondition for the loss of KJE. Both D. thermolithotrophum and T. ammonificans grow under strictly anaerobic conditions at temperatures in excess of 70°C, reminiscent of hyperthermophilic archaea, which--unlike their mesophilic cousins--also lack KJE. I suggest that high temperature promotes the evolution of high intrinsic protein solubility on a proteome-wide scale and thereby creates conditions under which KJE can be lost. However, the shift in solubility is common to all Aquificales and hence not sufficient to explain the restricted incidence of KJE loss.