Bacillus subtilis YqjG is required for genetic competence development

Proteomics

Volumn 11, Issue 2, 2011, Pages 270-282

  Saller, Manfred J ^a   Otto, Andreas ^b   Berrelkamp Lahpor, Greetje A ^a   Becher, Dörte ^b   Hecker, Michael ^b   Driessen, Arnold J M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Bacillus subtilis; Functional proteomics; Membrane proteins; Microbiology; Phage shock protein A; YidC

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; PROTEIN YQJG; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENETICS; BACTERIAL MEMBRANE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SPOROGENESIS; UNINDEXED SEQUENCE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; PROTEOME;

BACILLUS SUBTILIS;

EID: 78650771419     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000435     Document Type: Article

References (52)

1. Yen, M. R., Harley, K. T., Tseng, Y. H., Saier, M. H., Jr., Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol. Lett. 2001, 204, 223-231.
2. Jiang, F., Chen, M., Yi, L., de Gier, J. W. et al., Defining the regions of Escherichia coli YidC that contribute to activity. J. Biol. Chem. 2003, 278, 48965-48972.
3. Jia, L., Dienhart, M., Schramp, M., McCauley, M. et al., Yeast Oxa1 interacts with mitochondrial ribosomes: the importance of the C-terminal region of Oxa1. EMBO J. 2003, 22, 6438-6447.
4. Falk, S., Ravaud, S., Koch, J., Sinning, I., The C terminus of the Alb3 membrane insertase recruits cpSRP43 to the thylakoid membrane. J. Biol. Chem. 2010, 285, 5954-5962.
5. Kohler, R., Boehringer, D., Greber, B., Bingel-Erlenmeyer, R. et al., YidC and Oxa1 form dimeric insertion pores on the translating ribosome. Mol. Cell 2009, 34, 344-353.
6. O ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis. J. Cell Biol. 2004, 165, 213-222.
7. du Plessis, D. J., Nouwen, N., Driessen, A. J. M., Subunit a of cytochrome o oxidase requires both YidC and SecYEG for membrane insertion. J. Biol. Chem. 2006, 281, 12248-12252.
8. van Bloois, E., Haan, G. J., de Gier, J. W., Oudega, B. et al., Distinct requirements for translocation of the N-tail and C-tail of the Escherichia coli inner membrane protein CyoA. J. Biol. Chem. 2006, 281, 10002-10009.
9. van der Laan, M., Urbanus, M. L., ten Hagen-Jongman, C. M., Nouwen, N. et al., A conserved function of YidC in the biogenesis of respiratory chain complexes. Proc. Natl. Acad. Sci. USA 2003, 100, 5801-5806.
10. Facey, S. J., Neugebauer, S. A., Krauss, S., Kuhn, A., The mechanosensitive channel protein MscL is targeted by the SRP to the novel YidC membrane insertion pathway of Escherichia coli. J. Mol. Biol. 2007, 365, 995-1004.
11. O ATP synthase requires YidC and SecYEG for membrane insertion. J. Mol. Biol. 2009, 390, 893-901.
12. Price, C. E., Driessen, A. J., YidC is involved in the biogenesis of anaerobic respiratory complexes in the inner membrane of Escherichia coli. J. Biol. Chem. 2008, 283, 26921-26927.
13. Price, C. E., Driessen, A. J., Conserved negative charges in the transmembrane segments of subunit K of the NADH:ubiquinone oxidoreductase determine its dependence on YidC for membrane insertion. J. Biol. Chem. 2010, 285, 3575-3581.
14. Saller, M. J., Fusetti, F., Driessen, A. J., Bacillus subtilis SpoIIIJ and YqjG function in membrane protein biogenesis. J. Bacteriol. 2009, 191, 6749-6757.
15. O ATP synthase complex. Mol. Biol. Cell 2007, 18, 1897-1908.
16. Murakami, T., Haga, K., Takeuchi, M., Sato, T., Analysis of the Bacillus subtilis spoIIIJ gene and its paralogue gene, yqjG. J. Bacteriol. 2002, 184, 1998-2004.
17. Errington, J., Appleby, L., Daniel, R. A., Goodfellow, H. et al., Structure and function of the spoIIIJ gene of Bacillus subtilis: a vegetatively expressed gene that is essential for sigma G activity at an intermediate stage of sporulation. J. Gen. Microbiol. 1992, 138, 2609-2618.
18. Tjalsma, H., Bron, S., van Dijl, J. M., Complementary impact of paralogous Oxa1-like proteins of Bacillus subtilis on post-translocational stages in protein secretion. J. Biol. Chem. 2003, 278, 15622-15632.
19. Thomaides, H. B., Davison, E. J., Burston, L., Johnson, H. et al., Essential bacterial functions encoded by gene pairs. J. Bacteriol. 2007, 189, 591-602.
20. Chiba, S., Lamsa, A., Pogliano, K., A ribosome-nascent chain sensor of membrane protein biogenesis in Bacillus subtilis. EMBO J. 2009, 28, 3461-3475.
21. Stulke, J., Hanschke, R., Hecker, M., Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J. Gen. Microbiol. 1993, 139, 2041-2045.
22. Smits, W. K., Dubois, J. Y., Bron, S., van Dijl, J. M. et al., Tricksy business: transcriptome analysis reveals the involvement of thioredoxin A in redox homeostasis, oxidative stress, sulfur metabolism, and cellular differentiation in Bacillus subtilis. J. Bacteriol. 2005, 187, 3921-3930.
23. Bron, S., Venema, G., Ultraviolet inactivation and excision-repair in Bacillus subtilis. I. Construction and characterization of a transformable eightfold auxotrophic strain and two ultraviolet-sensitive derivatives. Mutat. Res. 1972, 15, 1-10.
24. Smits, W. K., Eschevins, C. C., Susanna, K. A., Bron, S. et al., Stripping Bacillus: ComK auto-stimulation is responsible for the bistable response in competence development. Mol. Microbiol. 2005, 56, 604-614.
25. Eymann, C., Dreisbach, A., Albrecht, D., Bernhardt, J. et al., A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 2004, 4, 2849-2876.
26. Dreisbach, A., Otto, A., Becher, D., Hammer, E. et al., Monitoring of changes in the membrane proteome during stationary phase adaptation of Bacillus subtilis using in vivo labeling techniques. Proteomics 2008, 8, 2062-2076.
27. Park, S. K., Venable, J. D., Xu, T., Yates, J. R., III A quantitative analysis software tool for mass spectrometry-based proteomics. Nat. Methods 2008, 5, 319-322.
28. MacCoss, M. J., Wu, C. C., Liu, H., Sadygov, R. et al., A correlation algorithm for the automated quantitative analysis of shotgun proteomics data. Anal. Chem. 2003, 75, 6912-6921.
29. Zhou, M., Boekhorst, J., Francke, C., Siezen, R. J., LocateP: genome-scale subcellular-location predictor for bacterial proteins. Biomed. Chromatogr. Bioinformatics 2008, 9, 173.
30. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., Candia, O. A., An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 1979, 100, 95-97.
31. Veening, J. W., Hamoen, L. W., Kuipers, O. P., Phosphatases modulate the bistable sporulation gene expression pattern in Bacillus subtilis. Mol. Microbiol. 2005, 56, 1481-1494.
32. Rubio, A., Jiang, X., Pogliano, K., Localization of translocation complex components in Bacillus subtilis: enrichment of the signal recognition particle receptor at early sporulation septa. J. Bacteriol. 2005, 187, 5000-5002.
33. Jordan, S., Junker, A., Helmann, J. D., Mascher, T., Regulation of LiaRS-dependent gene expression in Bacillus subtilis: identification of inhibitor proteins, regulator binding sites, and target genes of a conserved cell envelope stress-sensing two-component system. J. Bacteriol. 2006, 188, 5153-5166.
34. Kontinen, V. P., Sarvas, M., The PrsA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion. Mol. Microbiol. 1993, 8, 727-737.
35. Hsiao, T. L., Revelles, O., Chen, L., Sauer, U. et al., Automatic policing of biochemical annotations using genomic correlations. Nat. Chem. Biol. 2010, 6, 34-40.
36. Gyan, S., Shiohira, Y., Sato, I., Takeuchi, M. et al., Regulatory loop between redox sensing of the NADH/NAD(+) ratio by Rex (YdiH) and oxidation of NADH by NADH dehydrogenase Ndh in Bacillus subtilis. J. Bacteriol. 2006, 188, 7062-7071.
37. Meima, R., Eschevins, C., Fillinger, S., Bolhuis, A. et al., The bdbDC operon of Bacillus subtilis encodes thiol-disulfide oxidoreductases required for competence development. J. Biol. Chem. 2002, 277, 6994-7001.
38. Chen, I., Provvedi, R., Dubnau, D., A macromolecular complex formed by a pilin-like protein in competent Bacillus subtilis. J. Biol. Chem. 2006, 281, 21720-21727.
39. Jiang, F., Yi, L., Moore, M., Chen, M. et al., Chloroplast YidC homolog Albino3 can functionally complement the bacterial YidC depletion strain and promote membrane insertion of both bacterial and chloroplast thylakoid proteins. J. Biol. Chem. 2002, 277, 19281-19288.
40. Preuss, M., Ott, M., Funes, S., Luirink, J. et al., Evolution of mitochondrial oxa proteins from bacterial YidC. Inherited and acquired functions of a conserved protein insertion machinery. J. Biol. Chem. 2005, 280, 13004-13011.
41. van Bloois, E., Koningstein, G., Bauerschmitt, H., Herrmann, J. M. et al., Saccharomyces cerevisiae Cox18 complements the essential Sec-independent function of Escherichia coli YidC. FEBS J. 2007, 274, 5704-5713.
42. Wang, P., Kuhn, A., Dalbey, R. E., Global change of gene expression and cell physiology in YidC-depleted Escherichia coli. J. Bacteriol. 2010, 192, 2193-2209.
43. Camp, A. H. Losick, R., A novel pathway of intercellular signalling in Bacillus subtilis involves a protein with similarity to a component of type III secretion channels. Mol. Microbiol. 2008, 69, 402-417.
44. Serrano, M., Corte, L., Opdyke, J., Moran, C. P., Jr., et al., Expression of spoIIIJ in the prespore is sufficient for activation of sigma G and for sporulation in Bacillus subtilis. J. Bacteriol. 2003, 185, 3905-3917.
45. Serrano, M., Vieira, F., Moran, C. P., Jr., Henriques, A. O., Processing of a membrane protein required for cell-to-cell signaling during endospore formation in Bacillus subtilis. J. Bacteriol. 2008, 190, 7786-7796.
46. van Sinderen, D., Luttinger, A., Kong, L., Dubnau, D. et al., comK encodes the competence transcription factor, the key regulatory protein for competence development in Bacillus subtilis. Mol. Microbiol. 1995, 15, 455-462.
47. Antiporta, M. H., Dunny, G. M., ccfA, the genetic determinant for the cCF10 peptide pheromone in Enterococcus faecalis OG1RF. J. Bacteriol. 2002, 184, 1155-1162.
48. Hartl, B., Wehrl, W., Wiegert, T., Homuth, G. et al., Development of a new integration site within the Bacillus subtilis chromosome and construction of compatible expression cassettes. J. Bacteriol. 2001, 183, 2696-2699.
49. Guerout-Fleury, A. M., Shazand, K., Frandsen, N., Stragier, P., Antibiotic-resistance cassettes for Bacillus subtilis. Gene 1995, 167, 335-336.
50. O'Sullivan, D. J., Klaenhammer, T. R., High- and low-copy-number Lactococcus shuttle cloning vectors with features for clone screening. Gene 1993, 137, 227-231.
51. Bongers, R. S., Veening, J. W., Van Wieringen, M., Kuipers, O. P. et al., Development and characterization of a subtilin-regulated expression system in Bacillus subtilis: strict control of gene expression by addition of subtilin. Appl. Environ. Microbiol. 2005, 71, 8818-8824.
52. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A. M. et al., The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 1997, 390, 249-256.