Recent studies with Myxococcus xanthus have suggested that homologues of the Escherichia coli heat-shock sigma factor, RpoH, may not be involved in the heat-shock response in this δ-proteobacterium. The genome of another δ-proteobacterium, Geobacter sulfurreducens, which is considered to be a representative of the Fe(III)-reducing Geobacteraceae that predominate in a diversity of subsurface environments, contains an rpoH homologue. Characterization of the G. sulfurreducens rpoH homologue revealed that it was induced by a temperature shift from 30 °C to 42 °C and that an rpoH-deficient mutant was unable to grow at 42 °C. The predicted heat-shock genes, hrcA, grpE, dnaK, groES and htpG, were heat-shock inducible in an rpoH-dependent manner, and comparison of promoter regions of these genes identified the consensus sequences for the −10 and −35 promoter elements. In addition, DNA elements identical to the CIRCE consensus sequence were found in promoters of rpoH, hrcA and groES, suggesting that these genes are regulated by a homologue of the repressor HrcA, which is known to bind the CIRCE element. These results suggest that the G. sulfurreducens RpoH homologue is the heat-shock sigma factor and that heat-shock response in G. sulfurreducens is regulated positively by RpoH as well as negatively by the HrcA/CIRCE system.
BondD. R., HolmesD. E., TenderL. M.,
LovleyD. R.2002; Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485[CrossRef]
CoppiM. V., LeangC., SandlerS. J.,
LovleyD. R.2001; Development of a genetic system for Geobacter sulfurreducens . Appl Environ Microbiol 67:3180–3187[CrossRef]
GrossC. A.1996; Function and regulation of the heat shock proteins. In Escherichia coli and Salmonella: Cellular and Molecular Biology , 2nd edn. pp 1382–1399 Edited by NeidhardtF. C. and others Washington, DC: American Society for Microbiology;
MarxC. J.,
LidstromM. E.2001; Development of improved versatile broad-host-range vectors for use in methylotrophs and other Gram-negative bacteria. Microbiology 147:2065–2075
MethéB. A.,
NelsonK. E., EisenJ. A., PaulsenI. T., NelsonW., HeidelbergJ. F., WuD., WuM., WardN.
& other authors 2003; Genome of Geobacter sulfurreducens : metal reduction in subsurface environments. Science 302:1967–1969[CrossRef]
MogkA., HomuthG., ScholzC., KimL., SchmidF. X.,
SchumannW.1997; The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis . EMBO J 16:4579–4590[CrossRef]
NakahigashiK., YanagiH.,
YuraT.1995; Isolation and sequence analysis of rpoH genes encoding σ 32 from gram negative bacteria: conserved mRNA and protein segments for heat shock regulation. Nucleic Acids Res 23:4384–4390
NakahigashiK., RonE. Z., YanagiH.,
YuraT.1999; Differential and independent roles of a σ 32 homolog (RpoH) and an HrcA repressor in the heat shock response of Agrobacterium tumefaciens . J Bacteriol 181:7509–7515
NarberhausF., GiebelerK.,
BahlH.1992; Molecular characterization of the dnaK gene region of Clostridium acetobutylicum , including grpE , dnaJ , and a new heat shock gene. J Bacteriol 174:3290–3299
RodionovD. A., DubchakI., ArkinA., AlmE.,
GelfandM. S.2004; Reconstruction of regulatory and metabolic pathways in metal-reducing δ -proteobacteria. Genome Biol 5:R90[CrossRef]
SchulzA.,
SchumannW.1996; hrcA , the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J Bacteriol 178:1088–1093
TaylorW. E., StrausD. B., GrossmanA. D., BurtonZ. F., GrossC. A.,
BurgessR. R.1984; Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38:371–381[CrossRef]
UekiT.,
InouyeS.2001; SigB, SigC, and SigE from Myxococcus xanthus homologues to sigma 32 are not required for heat shock response but for multicellular differentiation. J Mol Microbiol Biotechnol 3:287–293
UekiT.,
InouyeS.2002; Transcriptional activation of a heat-shock gene, lonD , of Myxococcus xanthus by a two component histidine-aspartate phosphorelay system. J Biol Chem 277:6170–6177[CrossRef]
UekiT.,
InouyeS.2005; Identification of a gene involved in polysaccharide export as a transcription target of FruA, an essential factor for Myxococcus xanthus development. J Biol Chem 280:32279–32284[CrossRef]
WetzsteinM., VolkerU., DedioJ., LobauS., ZuberU., SchiesswohlM., HergetC., HeckerM.,
SchumannW.1992; Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis . J Bacteriol 174:3300–3310
YanB.,
UekiT.,
PuljicM., AdkinsR. M.,
LovleyD. R.,
KrushkalJ., NúñezC.,
Esteve-NúñezA.,
MethéB. A.2006; Computational prediction of RpoS and RpoD regulatory sites in Geobacter sulfurreducens using sequence and gene expression information. Gene 384:73–95[CrossRef]
YoungJ. C., AgasheV. R., SiegersK.,
HartlF. U.2004; Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5:781–791[CrossRef]
YuraT., KanemoriM.,
MoritaM. T.2000; The heat shock response: regulation and function. In Bacterial Stress Responses pp 3–18 Edited by
StorzG.Hengge-AronisR.
Washington, DC: American Society for Microbiology;
ZuberU.,
SchumannW.1994; CIRCE, a novel heat-shock element involved in regulation of heat-shock operon dnaK of Bacillus subtilis . J Bacteriol 176:1359–1363