Analysis of a Coxiella burnetti gene product that activates capsule synthesis in Escherichia coli: requirement for the heat shock chaperone DnaK and the two-component regulator RcsC

Zuber, Mohammed; Hoover, Timothy A.; Court, Donald L.

doi:10.1128/jb.177.15.4238-4244.1995

Cited by 40 publications

(47 citation statements)

References 34 publications

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“…A clue to a possible function emerged when it was shown that overexpression of DjlA could lead to the induction of a colanic acid capsule (17)(18)(19). Our observation that DjlA⌬TM, the DjlA 27-kDa cytoplasmic fragment, can function as a co-chaperone, in a manner identical to that of DnaJ, now strongly suggests that once produced in the cell in its native form, membraneanchored DjlA can engage and activate DnaK.…”

Section: Figmentioning

confidence: 92%

“…Thus, DjlA could represent a third DnaK co-chaperone in E. coli, but under what circumstances is unclear. A clue to a potential role for DjlA in the cell emerged in previous studies when we and others (17)(18)(19)(20) showed that DjlA overexpression could trigger the synthesis of a colanic acid polysaccharide capsule. In E. coli, a colanic acid capsule can be induced by environmental stress such as osmotic shock, low temperature, and desiccation (21)(22)(23).…”

mentioning

confidence: 99%

“…Previous genetic analyses of parameters affecting capsule induction revealed that activation of a wcaB-lacZ reporter by DjlA was abrogated in strains containing mutations in genes encoding the molecular chaperones DnaK and GrpE but was not adversely affected by null mutations in genes encoding DnaJ, CbpA, HtpG (Hsp90), or Hsc66 (Hsp70 homolog) (17,18). In the present work, we have used both biochemical and genetic analyses to address whether DjlA is a bona fide DnaK co-chaperone and whether direct DjlA-DnaK interaction is necessary for wca activation.…”

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DjlA Is a Third DnaK Co-chaperone of Escherichia coli, and DjlA-mediated Induction of Colanic Acid Capsule Requires DjlA-DnaK Interaction

Genevaux

Wawrzynów

Żylicz

et al. 2001

Journal of Biological Chemistry

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DjlA is a 30-kDa type III membrane protein of Escherichia coli with the majority, including an extreme Cterminal putative J-domain, oriented toward the cytoplasm. No other regions of sequence similarity aside from the J-domain exist between DjlA and the known DnaK (Hsp70) co-chaperones DnaJ (Hsp40) and CbpA. In this study, we explored whether and to what extent DjlA possesses DnaK co-chaperone activity and under what conditions a DjlA-DnaK interaction could be important to the cell. We found that the DjlA J-domain can substitute fully for the J-domain of DnaJ using various in vivo functional complementation assays. In addition, the purified cytoplasmic fragment of DjlA was shown to be capable of stimulating DnaK ATPase in a manner indistinguishable from DnaJ, and, furthermore, DjlA could act as a DnaK co-chaperone in the reactivation of chemically denatured luciferase in vitro. DjlA expression in the cell is tightly controlled, and even its mild overexpression leads to induction of mucoid capsule. Previous analysis showed that DjlA-mediated induction of the wca capsule operon required the RcsC/RcsB two-component signaling system and that wca induction by DjlA was lost when cells contained mutations in either the dnaK or grpE gene. We now show using allele-specific genetic suppression analysis that DjlA must interact with DnaK for DjlA-mediated stimulation of capsule synthesis. Collectively, these results demonstrate that DjlA is a co-chaperone for DnaK and that this chaperoneco-chaperone pair is implicated directly, or indirectly, in the regulation of colanic acid capsule.

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DjlA Is a Third DnaK Co-chaperone of Escherichia coli, and DjlA-mediated Induction of Colanic Acid Capsule Requires DjlA-DnaK Interaction

Genevaux

Wawrzynów

Żylicz

et al. 2001

Journal of Biological Chemistry

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“…Capsular polysaccharide expression and major cell envelope modifications appear to be a common theme of Rcs phosphorelay activation and it has been also proposed to play a role in regulating bacterial virulence and biofilm formation (Arricau et al, 1998;Ferrières & Clarke, 2003;Francez-Charlot et al, 2005;Tobe et al, 2005;Vianney et al, 2005). As yet the precise signal for pathway activation has not been determined, but it appears that the RcsC sensor responds to membrane perturbations such as osmotic stress, desiccation, bile salts and the aberrant expression of certain membrane-associated proteins (Ophir & Gutnick, 1994;Sledjeski & Gottesman, 1996;Clarke et al, 1997;Bernstein et al, 1999;Kelley & Georgopoulos, 1997;Potrykus & Wegrzyn, 2004;Zuber et al, 1995). Activation of this pathway has also been shown to occur during growth on a solid medium (Ferrières & Clarke, 2003).…”

Section: Introductionmentioning

confidence: 99%

The importance of the Rcs phosphorelay in the survival and pathogenesis of the enteropathogenic yersiniae

et al. 2008

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“…The mucZ gene product from C. burnetii induces capsule synthesis (mucoidy) when expressed in Escherichia coli (Zuber et al, 1995). MucZ proteins contain a C-terminal domain sharing significant similarity with the J domain of the bacterial Hsp40 cochaperone DnaJ, but are otherwise highly variable.…”

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16S rRNA-, GroEL- and MucZ-based assessment of the taxonomic position of 'Rickettsiella melolonthae' and its implications for the organization of the genus Rickettsiella

Leclerque¹,

Kleespies²

2008

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

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'Rickettsiella melolonthae' is an intracellularly multiplying bacterial pathogen of European cockchafers, Melolontha melolontha (Linnaeus, 1758) and Melolontha hippocastani (Fabricius, 1801) (Coleoptera: Scarabaeidae). We report the first determination of nucleotide sequences from this organism, i.e. the 16S rRNA encoding rrs gene, the chaperonin encoding groEL gene and the mucZ gene encoding the orthologue of a capsule synthesis-inducing factor of Coxiella burnetii. Within the genus Rickettsiella, the pathotype 'Rickettsiella melolonthae' is currently classified as a synonym of the nomenclatural type species Rickettsiella popilliae. Previous sequencing of a 16S rRNA gene from a different species, Rickettsiella grylli, has motivated the transfer of the entire genus from the alphaproteobacterial order Rickettsiales to the gammaproteobacterial order Legionellales, family Coxiellaceae. We investigated the validity of this taxonomic reorganization beyond the species Rickettsiella grylli by reconstructing the organismal phylogeny from comparisons of 16S rRNA gene and GroEL and MucZ protein sequences from a selected set of alpha-and gammaproteobacteria as well as bacterial pathogens from the order Chlamydiales. Our analysis strongly supported the transfer of the genus Rickettsiella to the order Legionellales, but not its classification in one of the recognized families present in this order. Furthermore, our results substantiated inconsistencies in the internal organization of the genus. In particular, the currently accepted delineation of Rickettsiella species and the claimed synonymy of 'Rickettsiella melolonthae' with Rickettsiella popilliae are not simultaneously consistent with our findings.The genus Rickettsiella (Philip, 1956) comprises intracellularly multiplying bacterial pathogens of insects, crustaceans and arachnids that were originally perceived as 'rickettsiae of insects ' (Dutky & Gooden, 1952;Krieg, 1955) and classified in the order Rickettsiales. An alternative assignment of these organisms to the order Chlamydiales has been judged less convincing (Weiss & Moulder, 1984). Within the genus Rickettsiella, there are currently four species with validly published names: the type species Rickettsiella popilliae (Dutky & Gooden, 1952), Rickettsiella grylli (Vago & Martoja, 1963), Rickettsiella chironomi (Weiser, 1963) and Rickettsiella stethorae (Hall & Badgley, 1957). However, according to Fournier & Raoult (2005), there is not sufficient evidence available to warrant the consideration of Rickettsiella stethorae as a distinct species. Numerous further pathotypes studied by electron microscopy have been suggested to represent synonyms of these species, while others still await conclusive species assignment. The pathotype 'Rickettsiella melolonthae' was discovered and first described as the causative agent of the 'Lorscher Erkrankung' (Lorsch disease) of white grubs of the European cockchafer species Melolontha melolontha (Linnaeus, 1758) and Melolontha hippocastani (Fabricius, 1801) (Coleoptera: Scarabaeidae...

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Analysis of a Coxiella burnetti gene product that activates capsule synthesis in Escherichia coli: requirement for the heat shock chaperone DnaK and the two-component regulator RcsC

Cited by 40 publications

References 34 publications

DjlA Is a Third DnaK Co-chaperone of Escherichia coli, and DjlA-mediated Induction of Colanic Acid Capsule Requires DjlA-DnaK Interaction

DjlA Is a Third DnaK Co-chaperone of Escherichia coli, and DjlA-mediated Induction of Colanic Acid Capsule Requires DjlA-DnaK Interaction

The importance of the Rcs phosphorelay in the survival and pathogenesis of the enteropathogenic yersiniae

16S rRNA-, GroEL- and MucZ-based assessment of the taxonomic position of 'Rickettsiella melolonthae' and its implications for the organization of the genus Rickettsiella

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