Complementation of Cold Shock Proteins by Translation Initiation Factor IF1 In Vivo

Abstract

The cold shock response in both Escherichia coli and Bacillus subtilis is induced by an abrupt downshift in growth temperature and leads to a dramatic increase in the production of a homologous class of small, often highly acidic cold shock proteins. This protein family is the prototype of the cold shock domain (CSD) that is conserved from bacteria to humans. For B. subtilis it has been shown that at least one of the three resident cold shock proteins (CspB to D) is essential under optimal growth conditions as well as during cold shock. Analysis of the B. subtilis cspB cspC double deletion mutant revealed that removal of these csp genes results in pleiotropic alteration of protein synthesis, cell lysis during the entry of stationary growth phase, and the inability to differentiate into endospores. We show here that heterologous expression of the translation initiation factor IF1 from E. coli in a B. subtilis cspB cspC double deletion strain is able to cure both the growth and the sporulation defects observed for this mutant, suggesting that IF1 and cold shock proteins have at least in part overlapping cellular function(s). Two of the possible explanation models are discussed.

Initiation of Protein Synthesis in Bacteria

“…It has been shown that the cellular defects resulting from a double deletion in the genes encoding cold shock proteins CspB and CspC in Bacillus subtilis can be complemented by heterologous expression of E. coli IF1 (244). This confirms the structural resemblance and functionality between IF1 and the cold shock proteins.…”

In vivo involvement of mutated initiation factor IF1 in gene expression control at the translational level

“…It has also been shown that heterologous expression of IF1 from E. coli in a Bacillus subtilis cspB/cspC double deletion strain complemented the loss of the cold shock induced protein CspB in B. subtilis (the homolog of CspA in E. coli) [36]. This finding led to a conclusion that IF1 and cold shock proteins have overlapping functions [36] and they could have evolved from a common ancestor [37]. Recently, it was shown that IF1 and CspA preferentially stimulate translation at low temperatures without mRNA selectivity [38] and that cold shock induces a stoichiometric imbalance between initiation factors and ribosomes [39].…”

Genomewide Transcriptional Analysis of the Cold Shock Response in Bacillus subtilis

“…The CSD is highly conserved from bacteria to humans (15,39,40) and is involved in coupling transcription to translation (36). Only recently the CSDBase database was established (http: //www.chemie.uni-marburg.de/ϳcsdbase), which includes detailed information about the CSD (37).…”

“…In B. subtilis, csp double-deletion strains show a variety of phenotypes, such as altered protein synthesis, aberrant nucleoid structure, cell lysis upon entry into the stationary growth phase, and impairment in sporulation (13,39). The latter two defects were shown to be cured by heterologous expression of translation initiation factor IF1 from Escherichia coli (36).…”