Spr1630 is Responsible for the Lethality of ClpX Mutations in Streptococcus Pneumoniae

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2009 May 26

PMID 19465654

Citations 7

Authors

Andrew Piotrowski

Peter Burghout

Donald A Morrison

Affiliations

Soon will be listed here.

Abstract

The Clp protease ATPase subunit and chaperone ClpX is dispensable in some bacteria, but it is thought to be essential in others, including streptococci and lactococci. We confirm that clpX is essential in the Rx strain of Streptococcus pneumoniae but show that the requirement for clpX can be relieved by point mutations, frame shifts, or deletion of the gene spr1630, which is found in many isolates of S. pneumoniae. Homologs occur frequently in Staphylococcus aureus as well as in a few strains of Listeria monocytogenes, Lactobacillus johnsonii, and Lactobacillus rhamnosus. In each case, the spr1630 homolog is accompanied by a putative transcriptional regulator with an HTH DNA binding motif. In S. pneumoniae, the spr1630-spr1629 gene pair, accompanied by a RUP element, occurs as an island inserted between the trpA and cclA genes in 15 of 22 sequenced genomes.

Citing Articles

A bacterial pan-genome makes gene essentiality strain-dependent and evolvable.

Rosconi F, Rudmann E, Li J, Surujon D, Anthony J, Frank M Nat Microbiol. 2022; 7(10):1580-1592.

PMID: 36097170 PMC: 9519441. DOI: 10.1038/s41564-022-01208-7.

Staphylococcus aureus ClpX localizes at the division septum and impacts transcription of genes involved in cell division, T7-secretion, and SaPI5-excision.

Jensen C, Fosberg M, Thalso-Madsen I, Baek K, Frees D Sci Rep. 2019; 9(1):16456.

PMID: 31712583 PMC: 6848492. DOI: 10.1038/s41598-019-52823-0.

Deciphering the distance to antibiotic resistance for the pneumococcus using genome sequencing data.

Mobegi F, Cremers A, de Jonge M, Bentley S, van Hijum S, Zomer A Sci Rep. 2017; 7:42808.

PMID: 28205635 PMC: 5311915. DOI: 10.1038/srep42808.

Temporal Regulation of the Transformasome and Competence Development in .

Zaccaria E, Wels M, van Baarlen P, Wells J Front Microbiol. 2017; 7:1922.

PMID: 28066332 PMC: 5167698. DOI: 10.3389/fmicb.2016.01922.

Characterization of pneumococcal Ser/Thr protein phosphatase phpP mutant and identification of a novel PhpP substrate, putative RNA binding protein Jag.

Ulrych A, Holeckova N, Goldova J, Doubravova L, Benada O, Kofronova O BMC Microbiol. 2016; 16(1):247.

PMID: 27776484 PMC: 5078927. DOI: 10.1186/s12866-016-0865-6.

References

Piotrowski A, Luo P, Morrison D . Competence for genetic transformation in Streptococcus pneumoniae: termination of activity of the alternative sigma factor ComX is independent of proteolysis of ComX and ComW. J Bacteriol. 2009; 191(10):3359-66. PMC: 2687157. DOI: 10.1128/JB.01750-08. View

Tettelin H, Nelson K, Paulsen I, Eisen J, Read T, Peterson S . Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science. 2001; 293(5529):498-506. DOI: 10.1126/science.1061217. View

Nakano S, Nakano M, Zhang Y, Leelakriangsak M, Zuber P . A regulatory protein that interferes with activator-stimulated transcription in bacteria. Proc Natl Acad Sci U S A. 2003; 100(7):4233-8. PMC: 153076. DOI: 10.1073/pnas.0637648100. View

Frees D, Savijoki K, Varmanen P, Ingmer H . Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, Gram-positive bacteria. Mol Microbiol. 2007; 63(5):1285-95. DOI: 10.1111/j.1365-2958.2007.05598.x. View

Gerth U, Kruger E, Derre I, Msadek T, Hecker M . Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol Microbiol. 1998; 28(4):787-802. DOI: 10.1046/j.1365-2958.1998.00840.x. View

Viala J, MAZODIER P . The ATPase ClpX is conditionally involved in the morphological differentiation of Streptomyces lividans. Mol Genet Genomics. 2003; 268(5):563-9. DOI: 10.1007/s00438-002-0783-1. View

Bijlsma J, Burghout P, Kloosterman T, Bootsma H, de Jong A, Hermans P . Development of genomic array footprinting for identification of conditionally essential genes in Streptococcus pneumoniae. Appl Environ Microbiol. 2007; 73(5):1514-24. PMC: 1828782. DOI: 10.1128/AEM.01900-06. View

Jones J, Welty D, Nakai H . Versatile action of Escherichia coli ClpXP as protease or molecular chaperone for bacteriophage Mu transposition. J Biol Chem. 1998; 273(1):459-65. DOI: 10.1074/jbc.273.1.459. View

Liu J, Cosby W, Zuber P . Role of lon and ClpX in the post-translational regulation of a sigma subunit of RNA polymerase required for cellular differentiation in Bacillus subtilis. Mol Microbiol. 1999; 33(2):415-28. DOI: 10.1046/j.1365-2958.1999.01489.x. View

10.

Levchenko I, Luo L, Baker T . Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev. 1995; 9(19):2399-408. DOI: 10.1101/gad.9.19.2399. View

11.

Frees D, Sorensen K, Ingmer H . Global virulence regulation in Staphylococcus aureus: pinpointing the roles of ClpP and ClpX in the sar/agr regulatory network. Infect Immun. 2005; 73(12):8100-8. PMC: 1307069. DOI: 10.1128/IAI.73.12.8100-8108.2005. View

12.

Turgay K, Hahn J, Burghoorn J, Dubnau D . Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. EMBO J. 1999; 17(22):6730-8. PMC: 1171018. DOI: 10.1093/emboj/17.22.6730. View

13.

Msadek T, Dartois V, Kunst F, Herbaud M, Denizot F, Rapoport G . ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol Microbiol. 1998; 27(5):899-914. DOI: 10.1046/j.1365-2958.1998.00735.x. View

14.

Clarke A, Schelin J, Porankiewicz J . Inactivation of the clpP1 gene for the proteolytic subunit of the ATP-dependent Clp protease in the cyanobacterium Synechococcus limits growth and light acclimation. Plant Mol Biol. 1998; 37(5):791-801. DOI: 10.1023/a:1006016302074. View

15.

Gottesman S . Regulation by proteolysis: developmental switches. Curr Opin Microbiol. 1999; 2(2):142-7. DOI: 10.1016/S1369-5274(99)80025-3. View

16.

Oggioni M, Claverys J . Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae. Microbiology (Reading). 1999; 145 ( Pt 10):2647-53. DOI: 10.1099/00221287-145-10-2647. View

17.

KENT J, HOTCHKISS R . KINETIC ANALYSIS OF MULTIPLE, LINKED RECOMBINATIONS IN PNEUMOCOCCAL TRANSFORMATION. J Mol Biol. 1964; 9:308-22. DOI: 10.1016/s0022-2836(64)80209-6. View

18.

Robertson G, Ng W, Foley J, Gilmour R, Winkler M . Global transcriptional analysis of clpP mutations of type 2 Streptococcus pneumoniae and their effects on physiology and virulence. J Bacteriol. 2002; 184(13):3508-20. PMC: 135132. DOI: 10.1128/JB.184.13.3508-3520.2002. View

19.

Weart R, Nakano S, Lane B, Zuber P, Levin P . The ClpX chaperone modulates assembly of the tubulin-like protein FtsZ. Mol Microbiol. 2005; 57(1):238-49. PMC: 5432201. DOI: 10.1111/j.1365-2958.2005.04673.x. View

20.

Lemos J, Burne R . Regulation and Physiological Significance of ClpC and ClpP in Streptococcus mutans. J Bacteriol. 2002; 184(22):6357-66. PMC: 151938. DOI: 10.1128/JB.184.22.6357-6366.2002. View