Eubacterial SpoVG Homologs Constitute a New Family of Site-Specific DNA-Binding Proteins

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Jutras, Brandon L ^a   Chenail, Alicia M ^a   Rowland, Christi L ^b   Carroll, Dustin ^a   Miller, M Clarke ^c   Bykowski, Tomasz ^a   Stevenson, Brian ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA BINDING PROTEIN; SPOVG PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BORRELIA BURGDORFERI; CONTROLLED STUDY; CYTOPLASM; DNA SEQUENCE; EUBACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; STAPHYLOCOCCUS AUREUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BINDING, COMPETITIVE; BORRELIA BURGDORFERI; DNA, BACTERIAL; DNA-BINDING PROTEINS; EUBACTERIUM; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEOTIDE MOTIFS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI; STAPHYLOCOCCUS AUREUS;

EID: 84879253115     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066683     Document Type: Article

References (51)

1. Bykowski T, Babb K, von Lackum K, Riley SP, Norris SJ, et al. (2006) Transcriptional regulation of the Borrelia burgdorferi antigenically variable VlsE surface protein. J Bacteriol 188: 4879-4889.
2. Norris SJ, (2006) Antigenic variation with a twist- the Borrelia story. Mol Microbiol 60: 1319-1322.
3. Margolis PS, Driks A, Losick R, (1993) Sporulation gene spoIIB from Bacillus subtilis. J Bacteriol 175: 528-540.
4. Matsuno K, Sonenshein AL, (1999) Role of SpoVG in asymmetric septation in Bacillus subtilis. J Bacteriol 181: 3392-3401.
5. Resnekov O, Driks A, Losick R, (1995) Identification and characterization of sporulation gene spoVS from Bacillus subtilis. J Bacteriol 177: 5628-5635.
6. Perez AR, Abanes-De Mello A, Pogliano K (2000) SpoIIB localizes to active sites of septal biogenesis and spatially regulates septal thinning during engulfment in Bacillus subtilis. J Bacteriol 182.
7. Perez AR, Abanes-De Mello A, Pogliano K, (2006) Suppression of engulfment defects in Bacillus subtilis by elevated expression of the motility regulon. J Bacteriol 188: 1159-1164.
8. Schulthess B, Meier S, Homerova D, Goerke C, Wolz C, et al. (2009) Functional characterization of the σB-dependent yabJ-spoVG operon in Staphylococcus aureus: role in methicillin and glycopeptide resistance. Antimicrob Agents Chemother 53: 1832-1839.
9. Schulthess B, Bloes DA, François P, Girard M, Schrenzel J, et al. (2011) The σB-dependent yabJ-spoVG operon is involved in the regulation of extracellular nuclease, lipase, and protease expression in Staphylococcus aureus. J Bacteriol 193: 4954-4962.
10. Schulthess B, Bloes DA, Berger-Bächi B, (2012) Opposing roles of σB and σB-controlled SpoVG in the global regulation of esxA in Staphylococcus aureus. BMC Microbiol 24: 12-17.
11. Bischoff M, Dunman P, Kormanec J, Macapagal D, Murphy E, et al. (2004) Microarray-based analysis of the Staphylococcus aureus σB regulon. J Bacteriol 186: 4085-4099.
12. Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, et al. (2002) Genome-wide analysis of the stationary-phase sigma factor (Sigma-H) regulon of Bacillus subtilis. J Bacteriol 184: 4881-4890.
13. Fürbass R, Gocht M, Zuber P, Marahiel MA, (1991) Interaction of AbrB, a transcriptional regulator from Bacillus subtilis with the promoters of the transition state-activated genes tycA and spoVG. Mol Gen Genet 225: 347-354.
14. Hadjifrangiskou M, Chen Y, Koehler TM, (2007) The alternative sigma factor sigmaH is required for toxin gene expression by Bacillus anthracis. J Bacteriol 189: 1874.
15. Haldenwang WG, Losick R, (1979) A modified RNA polymerase transcribes a cloned gene under sporulation control in Bacillus subtilis. Nature 282: 256-260.
16. Johnson WC, Moran CP, Losick R, (1983) Two RNA polymerase sigma factors from Bacillus subtilis discriminate between overlapping promoters for a developmentally regulated gene. Nature 302: 800-804.
17. Meier S, Goerke C, Wolz C, Seidl K, Homerova D, et al. (2007) σB and the σB-dependent arlRS and yabJspoVG loci affect capsule formation in Staphylococcus aureus. Infect Immun 75: 4562-4571.
18. Robertson JB, Gocht M, Marahiel MA, Zuber P, (1989) AbrB, a regulator of gene expression in Bacillus, interacts with the transcription initiation regions of a sporulation gene and an antibiotic biosynthesis gene. Proc Natl Acad Sci 86: 8457-8461.
19. Rosenbluh A, Banner CD, Losick R, Fitz-James PC, (1981) Identification of a new developmental locus in Bacillus subtilis by construction of a deletion mutation in a cloned gene under sporulation control. J Bacteriol 148: 341-351.
20. Saujet L, Monot M, Dupuy B, Soutourina O, Martin-Verstraete I, (2011) The key sigma factor of transition phase, SigH, controls sporulation, metabolism, and virulence factor expression in Clostridium difficile. J Bacteriol 193: 3186-3196.
21. Segall J, Losick R, (1977) Cloned Bacillus subtilis DNA containing a gene that is activated early during sporulation. Cell 11: 751-761.
22. Zuber P, Losick R, (1983) Use of a lacZ fusion to study the role of the spoO genes of Bacillus subtilis in developmental regulation. Cell 35: 275-283.
23. Chaffin DO, Taylor D, Skerrett SJ, Rubens CE, (2012) Changes in the Staphylococcus aureus transcriptome during early adaptation to the lung. PLoS ONE 7: e41329.
24. Kim HH, Lee BJ, Kwon AR, (2010) Expression, crystallization, and preliminary X-ray crystallographic analysis of putative SpoVG from Staphylococcus aureus. Arch Pharm Res 33: 1285-1288.
25. Babb K, Bykowski T, Riley SP, Miller MC, DeMoll E, et al. (2006) Borrelia burgdorferi EbfC, a novel, chromosomally-encoded protein, binds specific DNA sequences adjacent to erp loci on the spirochete's resident cp32 prophages. J Bacteriol 188: 4331-4339.
26. Burns LH, Adams CA, Riley SP, Jutras BL, Bowman A, et al. (2010) BpaB, a novel protein encoded by the Lyme disease spirochete's cp32 prophages, binds to erp Operator 2 DNA. Nucleic Acids Res 38: 5443-5455.
27. Jutras BL, Verma A, Stevenson B (2012) Identification of novel DNA-binding proteins using DNA-affinity chromatography/pull down. Curr Protocols Microbiol: 1F.1.1-13.
28. Babb K, McAlister JD, Miller JC, Stevenson B, (2004) Molecular characterization of Borrelia burgdorferi erp promoter/operator elements. J Bacteriol 186: 2745-2756.
29. Jutras BL, Verma A, Adams CA, Brissette CA, Burns LH, et al. (2012) BpaB and EbfC DNA-binding proteins regulate production of the Lyme disease spirochete's infection-associated Erp surface proteins. J Bacteriol 194: 778-786.
30. Grove A, (2011) Functional evolution of bacterial histone-like HU proteins. Curr Issues Mol Biol 13: 1-12.
31. Luscombe NM, Laskowski RA, Thornton JM, (2001) Amino acid-base interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucl Acids Res 29: 2860-2874.
32. Ohniwa RL, Ushijima Y, Saito S, Morikawa K, (2011) Proteomic analyses of nucleoid-associated proteins in Escherichia coli, Pseudomonas aeruginosa, Bacillus subtilis, and Staphylococcus aureus. PLoS ONE 4: e19172.
33. Capra EJ, Perchuk BS, Lubin EA, Ashenberg O, Skerker JM, et al. (2010) Systematic dissection and trajectory-scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways. PLoS Genet 6: e1001220.
34. Capra EJ, Perchuk BS, Skerker JM, Laub MT, (2012) Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell 150: 222-232.
35. Capra EJ, Laub MT, (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66: 325-347.
36. Cocchiaro JL, Gomez MI, Risley A, Solinga R, Sordelli DO, et al. (2006) Molecular characterization of the capsule locus from non-typeable Staphylococcus aureus. Mol Microbiol 59: 948-960.
37. Luong T, Sau S, Gomez M, Lee JC, Lee CY, (2002) Regulation of Staphylococcus aureus capsular polysaccharide expression by agr and sarA. Infect Immun 70: 444-450.
38. Luong TT, Lee CY, (2006) The arl locus positively regulates Staphylococcus aureus type 5 capsule via an mgrA-dependent pathway. Microbiology 152: 3123-3131.
39. Luong TT, Sau K, Roux C, Sau S, Dunman PM, et al. (2011) Staphylococcus aureus ClpC divergently regulates capsule via sae and codY in strain newman but activates capsule via codY in strain UAMS-1 and in strain Newman with repaired saeS. J Bacteriol 193: 686-694.
40. Majerczyk CD, Dunman PM, Luong TT, Lee CY, Sadykov MR, et al. (2010) Direct targets of CodY in Staphylococcus aureus. J Bacteriol 192: 2861-2877.
41. Zhang JR, Hardham JM, Barbour AG, Norris SJ, (1997) Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89: 1-20.
42. Dresser AR, Hardy PO, Chaconas G, (2009) Investigation of the genes involved in antigenic switching at the vlsE locus in Borrelia burgdorferi: An essential role for the RuvAB branch migrase. PLoS Pathog 5: e1000680.
43. Liveris D, Mulay V, Sandigursky S, Schwartz I, (2008) Borrelia burgdorferi vlsE antigenic variation is not mediated by RecA. Infect Immun 76: 4009-4018.
44. Walia R, Chaconas G, (2013) Suggested role for G4 DNA in recombinational switching at the antigenic variation locus of the Lyme disease spirochete. PLoS ONE 8: e57792.
45. Zückert WR, (2007) Laboratory maintenance of Borrelia burgdorferi. Curr Protocols Microbiol 12C: 1-10.
46. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
47. Casjens S, Palmer N, van Vugt R, Huang WM, Stevenson B, et al. (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs of an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35: 490-516.
48. Chenail AM, Jutras BL, Adams CA, Burns LH, Bowman A, et al. (2012) Borrelia burgdorferi cp32 BpaB modulates expression of the prophage NucP nuclease and SsbP single-stranded DNA-binding protein. J Bacteriol 194: 4570-4578.
49. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR, (1989) Site-directed mutagensis by overlap extension using polymerase chain reaction. Gene 77: 51-59.
50. Riley SP, T. Bykowski T, Cooley AE, Burns LH, Babb K, et al. (2009) Borrelia burgdorferi EbfC defines a newly-identified, widespread family of bacterial DNA-binding proteins. Nucleic Acids Res 37: 1973-1983.
51. Willems A, Collins MD, (1995) 16s rRNA gene similarities indicate that Hallella seregens (Moore and Moore) and Mitsuokella dentalis (Haapasalo et al.) are genealogically highly related and are members of the Genus Prevotella: emended description of the Genus Prevotella (Shah and Collins) and description of Prevotella dentalis comb. nov. Int J Syst Bacteriol 45: 832-836.