Far from being well understood: Multiple protein phosphorylation events control cell differentiation in Bacillus subtilis at different levels

Frontiers in Microbiology

Volumn 5, Issue DEC, 2014, Pages

  Gerwig, Jan ^a   Stülke, Jörg ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Biofilm formation; Cross talk; EpsB; PtkA; Tyrosine phosphorylation

Indexed keywords

BACTERIAL POLYSACCHARIDE; PHOSPHOPROTEIN; PHOSPHOTRANSFERASE; PROTEIN TYROSINE KINASE;

BACILLUS SUBTILIS; CELL DIFFERENTIATION; MICROBIAL COMMUNITY; NONHUMAN; NOTE; PHOSPHORYLATION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

BACILLUS SUBTILIS;

EID: 84920670439     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00704     Document Type: Note

References (34)

1. Baer, C. E., Iavarone, A. T., Alber, T., and Sassetti, C. M. (2014). Biochemical and spatial coincidence in the provisional Ser/Thr protein kinase interaction network of Mycobacterium tuberculosis. J. Biol. Chem. 289, 20422-20433. doi: 10.1074/jbc.M114.559054
2. Beauregard, P. B., Chai, Y., Vlamakis, H., Losick, R., and Kolter, R. (2013). Bacillus subtilis biofilm induction by plant polysaccharides. Proc. Natl. Acad. Sci. U.S.A. 110, E1621-E1630. doi: 10.1073/pnas.1218984110
3. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322. doi: 10.1126/science.284.5418.1318
4. Derouiche, A., Bidnenko, V., Grenha, R., Pigonneau, N., Ventroux, M., Franz-Wachtel, M., et al. (2013). Interaction of bacterial fatty-acid-displaced regulators with DNA is interrupted by tyrosine phosphorylation in the helix-turn-helix domain. Nucleic Acids Res. 41, 9371-9381. doi: 10.1093/nar/gkt709
5. Elsholz, A. K. W., Wacker, S. A., and Losick, R. (2014). Self-regulation of exopolysaccharide production in Bacillus subtilis by a tyrosine kinase. Genes Dev. 28, 1710-1720. doi: 10.1101/gad.246397.114
6. Fujita, M., González-Pastor, J. E., and Losick, R. (2005). High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J. Bacteriol. 187, 1357-1368. doi: 10.1128/JB.187.4.1357-1368.2005
7. Fujita, M., and Losick, R. (2005). Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev. 19, 2236-2244. doi: 10.1101/gad.1335705
8. Gerwig, J., Kiley, T. B., Gunka, K., Stanley-Wall, N., and Stülke, J. (2014). The protein tyrosine kinases EpsB and PtkA differentially affect biofilm formation in Bacillus subtilis. Microbiology 160, 682-691. doi: 10.1099/mic.0.074971-0
9. Grangeasse, C., Nessler, S., and Mijakovic, I. (2012). Bacterial tyrosine kinases: evolution, biological function and structural insights. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 367, 2640-2655. doi: 10.1098/rstb.2011.0424
10. Guttenplan, S. B., Blair, K. M., and Kearns, D. B. (2010). The EpsE flagellar clutch is bifunctional and synergizes with EPS biosynthesis to promote Bacillus subtilis biofilm formation. PLoS Genet. 6:e1001243. doi: 10.1371/journal.pgen.1001243
11. Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95-108. doi: 10.1038/nrmicro821
12. Hübner, S., Declerck, N., Diethmaier, C., Le Coq, D., Aymerich, S., and Stülke, J. (2011). Prevention of cross-talk in conserved regulatory systems: Identification of specificity determinants in RNA-binding antitermination proteins of the BglG family. Nucleic Acids Res. 39, 4360-4372. doi: 10.1093/nar/gkr021
13. Jers, C., Pedersen, M. M., Paspaliari, D. K., Schütz, W., Johnsson, C., Soufi, B., et al. (2010). Bacillus subtilis BY-kinase PtkA controls enzyme activity and localization of its protein substrates. Mol. Microbiol. 77, 287-299. doi: 10.1111/j.1365-2958.2010.07227.x
14. Kearns, D. B., Chu, F., Branda, S. S., Kolter, R., and Losick, R. (2005). A master regulator for biofilm formation by Bacillus subtilis. Mol. Microbiol. 55, 739-749. doi: 10.1111/j.1365-2958.2004.04440.x
15. Kiley, T. B., and Stanley-Wall, N. R. (2010). Post-translational control of Bacillus subtilis biofilm formation mediated by tyrosine phosphorylation. Mol. Microbiol. 78, 947-963. doi: 10.1111/j.1365-2958.2010.07382.x
16. Kobir, A., Poncet, S., Bidnenko, V., Delumeau, O., Jers, C., Zouhir, S., et al. (2014). Phosphorylation of Bacillus subtilis gene regulator AbrB modulates its DNA-binding properties. Mol. Microbiol. 92, 1129-1141. doi: 10.1111/mmi.12617
17. Kolodkin-Gal, I., Elsholz, A. K. W., Muth, C., Girguis, P. R., Kolter, R., and Losick, R. (2013). Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase. Genes Dev. 27, 887-899. doi: 10.1101/gad.215244.113
18. López, D., Fischbach, M. A., Chu, F., Losick, R., and Kolter, R. (2009). Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 106, 280-285. doi: 10.1073/pnas.0810940106
19. López, D., and Kolter, R. (2010). Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol. Rev. 34, 134-149. doi: 10.1111/j.1574-6976.2009.00199.x
20. Macek, B., Mijakovic, I., Olsen, J. V., Gnad, F., Kumar, C., Jensen, P. R., et al. (2007). The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol. Cell. Proteomics 6, 697-707. doi: 10.1074/mcp.M600464-MCP200
21. Marlow, V. L., Cianfanelli, F. R., Porter, M., Cairns, L. S., Dale, J. K., and Stanley-Wall, N. R. (2014). The prevalence and origin of exoprotease-producing cells in the Bacillus subtilis biofilm. Microbiology 160, 56-66. doi: 10.1099/mic.0.072389-0
22. Mhatre, E., Monterrosa, R. G., and Kovács, A. T. (2014). From environmental signals to regulators: modulation of biofilm development in Gram-positive bacteria. J. Basic Microbiol. 54, 616-632. doi: 10.1002/jobm.201400175
23. Mielich-Süss, B., and Lopez, D. (2014). Molecular mechanisms involved in Bacillus subtilis biofilm formation. Environ. Microbiol. doi: 10.1111/1462-2920.12527. [Epub ahead of print].
24. Mijakovic, I., Petranovic, D., Macek, B., Cepo, T., Mann, M., Davies, J., et al. (2006). Bacterial single-stranded DNA-binding proteins are phosphorylated on tyrosine. Nucleic Acids Res. 34, 1588-1596. doi: 10.1093/nar/gkj514
25. Newman, J. A., Rodrigues, C., and Lewis, R. J. (2013). Molecular basis of the activity of SinR protein, the master regulator of biofilm formation in Bacillus subtilis. J. Biol. Chem. 288, 10766-10778. doi: 10.1074/jbc.M113.455592
26. Podgornaia, A. I., and Laub, M. T. (2013). Determinants of specificity in two-component signal transduction. Curr. Opin. Microbiol. 16, 156-162. doi: 10.1016/j.mib.2013.01.004
27. Ravikumar, V., Shi, L., Krug, K., Derouiche, A., Jers, C., Cousin, C., et al. (2014). Quantitative phosphoproteome analysis of Bacillus subtilis reveals novel substrates of the kinase PrkC and phosphatase PrpC. Mol. Cell. Proteomics 13, 1965-1978. doi: 10.1074/mcp.M113.035949
28. Schilling, O., Herzberg, C., Hertrich, T., Vörsmann, H., Jessen, D., Hübner, S., et al. (2006). Keeping signals straight in transcription regulation: specificity determinants for the interaction of a family of conserved bacterial RNA-protein couples. Nucleic Acids Res. 34, 6102-6115. doi: 10.1093/nar/gkl733
29. Shi, L., Pigeonneau, N., Ravikumar, V., Dobrinic, P., Macek, B., Franjevic, D., et al. (2014). Cross-phosphorylation of bacterial serine/threonine and tyrosine protein kinases on key regulatory residues. Front. Microbiol. 5:495. doi: 10.3389/fmicb.2014.00495
30. Soulat, D., Grangeasse, C., Vaganay, E., Cozzone, A. J., and Duclos, B. (2007). UDP-acetyl-mannosamine dehydrogenase is an endogenous protein substrate of Staphylococcus aureus protein-tyrosine kinase activity. J. Mol. Microbiol. Biotechnol. 13, 45-54. doi: 10.1159/000103596
31. Szurmant, H., and Hoch, J. A. (2010). Interaction fidelity in two-component signaling. Curr. Opin. Microbiol. 13, 190-197. doi: 10.1016/j.mib.2010.01.007
32. van Noort, V., Seebacher, J., Bader, S., Mohammed, S., Vonkova, I., Betts, M. J., et al. (2012). Cross-talk between phosphorylation and lysine acetylation in a genome-reduced bacterium. Mol. Syst. Biol. 8, 571. doi: 10.1038/msb.2012.4
33. Vlamakis, H., Chai, Y., Beauregard, P., Losick, R., and Kolter, R. (2013). Sticking together: building a biofilm the Bacillus subtilis way. Nat. Rev. Microbiol. 11, 157-168. doi: 10.1038/nrmicro2960
34. Winkelman, J. T., Bree, A. C., Bate, A. R., Eichenberger, P., Gourse, R. L., and Kearns, D. B. (2013). RemA is a DNA-binding protein that activates biofilm matrix gene expression in Bacillus subtilis. Mol. Microbiol. 88, 984-997. doi: 10.1111/mmi.12235