The Sinorhizobium meliloti sensor histidine kinase CbrA contributes to free-living cell cycle regulation

Microbiology (United Kingdom)

Volumn 159, Issue 8, 2013, Pages 1552-1563

  Sadowsk, Craig S ^a   Wilson, Daniel ^a,c   Schallies, Karla B ^a   Walker, Graham ^b   Gibson, Katherine E ^a  

^a UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c Regents Hall of Natural Science and Mathematics ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHLORAMPHENICOL; DNA; EXOPOLYSACCHARIDE; GENTAMICIN; KANAMYCIN; NEOMYCIN; OXYTETRACYCLINE; PROTEIN CBRA; PROTEIN HISTIDINE KINASE; RIFAMPICIN; STREPTOMYCIN; TETRACYCLINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; CAULOBACTER CRESCENTUS; CELL CYCLE REGULATION; CELL DIVISION; CELL FATE; CELL GROWTH; CELL STRUCTURE; CONTROLLED STUDY; DNA REPLICATION; ENZYME PHOSPHORYLATION; GRAM NEGATIVE BACTERIUM; MOLECULAR MECHANICS; NONHUMAN; PHYLOGENY; POLAR BODY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SINORHIZOBIUM MELILOTI; STEADY STATE; SYMBIOSIS; WILD TYPE;

CAULOBACTER CRESCENTUS; CELL CYCLE; CELL CYCLE PROTEINS; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID; SINORHIZOBIUM MELILOTI;

EID: 84881257867     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.067504-0     Document Type: Article

References (63)

1. Barnett, M. J., Hung, D. Y., Reisenauer, A., Shapiro, L. & Long, S. R. (2001). A homolog of the CtrA cell cycle regulator is present and essential in Sinorhizobium meliloti. J Bacteriol 183, 3204-3210.
2. Bastedo, D. P. & Marczynski, G. T. (2009). CtrA response regulator binding to the Caulobacter chromosome replication origin is required during nutrient and antibiotic stress as well as during cell cycle progression. Mol Microbiol 72, 139-154.
3. Bellefontaine, A. F., Pierreux, C. E., Mertens, P., Vandenhaute, J., Letesson, J. J. & De Bolle, X. (2002). Plasticity of a transcriptional regulation network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus. Mol Microbiol 43, 945-960.
4. Bina, J. E. & Mekalanos, J. J. (2001). Vibrio cholerae tolC is required for bile resistance and colonization. Infect Immun 69, 4681-4685.
5. Biondi, E. G., Reisinger, S. J., Skerker, J. M., Arif, M., Perchuk, B. S., Ryan, K. R. & Laub, M. T. (2006). Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444, 899-904.
6. Brilli, M., Fondi, M., Fani, R., Mengoni, A., Ferri, L., Bazzicalupo, M. & Biondi, E. G. (2010). The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis. BMC Syst Biol 4, 52.
7. Brown, P. J., de Pedro, M. A., Kysela, D. T., Van der Henst, C., Kim, J., De Bolle, X., Fuqua, C. & Brun, Y. V. (2012). Polar growth in the Alphaproteobacterial order Rhizobiales. Proc Natl Acad Sci U S A 109, 1697-1701.
8. Chen, Y. E., Tsokos, C. G., Biondi, E. G., Perchuk, B. S. & Laub, M. T. (2009). Dynamics of two phosphorelays controlling cell cycle progression in Caulobacter crescentus. J Bacteriol 191, 7417-7429.
9. Chen, Y. E., Tropini, C., Jonas, K., Tsokos, C. G., Huang, K. C. & Laub, M. T. (2011). Spatial gradient of protein phosphorylation underlies replicative asymmetry in a bacterium. Proc Natl Acad Sci U S A 108, 1052-1057.
10. Cheng, H. P. & Walker, G. C. (1998). Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI twocomponent regulatory system. J Bacteriol 180, 20-26.
11. Cheng, J., Sibley, C. D., Zaheer, R. & Finan, T. M. (2007). A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis. Microbiology 153, 375-387.
12. Curtis, P. D. & Brun, Y. V. (2010). Getting in the loop: regulation of development in Caulobacter crescentus. MicrobiolMol Biol Rev 74, 13-41.
13. Curtis, P. D., Quardokus, E. M., Lawler, M. L., Guo, X., Klein, D., Chen, J. C., Arnold, R. J. & Brun, Y. V. (2012). The scaffolding and signaling functions of a localization factor impact polar development. Mol Microbiol 84, 712-735.
14. Domenech, P., Kobayashi, H., LeVier, K., Walker, G. C. & Barry, C. E., III (2009). BacA, an ABC transporter involved in maintenance of chronic murine infections with Mycobacterium tuberculosis. J Bacteriol 191, 477-485.
15. Domian, I. J., Quon, K. C. & Shapiro, L. (1997). Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90, 415-424.
16. Ehrhardt, D. W., Atkinson, E. M. & Long, S. R. (1992). Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256, 998-1000.
17. Fields, A. T., Navarrete, C. S., Zare, A. Z., Huang, Z., Mostafavi, M., Lewis, J. C., Rezaeihaghighi, Y., Brezler, B. J., Ray, S. & other authors (2012). The conserved polarity factor podJ1 impacts multiple cell envelope-associated functions in Sinorhizobium meliloti. Mol Microbiol 84, 892-920.
18. Finan, T. M., Hartweig, E., LeMieux, K., Bergman, K., Walker, G. C. & Signer, E. R. (1984). General transduction in Rhizobium meliloti. J Bacteriol 159, 120-124.
19. Gibson, K. E., Campbell, G. R., Lloret, J. & Walker, G. C. (2006). CbrA is a stationary-phase regulator of cell surface physiology and legume symbiosis in Sinorhizobium meliloti. J Bacteriol 188, 4508-4521.
20. Gibson, K. E., Barnett, M. J., Toman, C. J., Long, S. R. & Walker, G. C. (2007). The symbiosis regulator CbrA modulates a complex regulatory network affecting the flagellar apparatus and cell envelope proteins. J Bacteriol 189, 3591-3602.
21. Gibson, K. E., Kobayashi, H. & Walker, G. C. (2008). Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42, 413-441.
22. Haag, A. F., Baloban, M., Sani, M., Kerscher, B., Pierre, O., Farkas, A., Longhi, R., Boncompagni, E., Herouart, D. & other authors (2011). Protection of Sinorhizobium against host cysteine-rich antimicrobial peptides is critical for symbiosis. PLoS Biol 9, e1001169.
23. Hallez, R., Bellefontaine, A. F., Letesson, J. J. & De Bolle, X. (2004). Morphological and functional asymmetry in a-proteobacteria. Trends Microbiol 12, 361-365.
24. Hallez, R., Mignolet, J., Van Mullem, V., Wery, M., Vandenhaute, J., Letesson, J. J., Jacobs-Wagner, C. & De Bolle, X. (2007). The asymmetric distribution of the essential histidine kinase PdhS indicates a differentiation event in Brucella abortus. EMBO J 26, 1444-1455.
25. Hecht, G. B., Lane, T., Ohta, N., Sommer, J. M. & Newton, A. (1995). An essential single domain response regulator required for normal cell division and differentiation in Caulobacter crescentus. EMBO J 14, 3915-3924.
26. Hung, D. Y. & Shapiro, L. (2002). A signal transduction protein cues proteolytic events critical to Caulobacter cell cycle progression. Proc Natl Acad Sci U S A 99, 13160-13165.
27. Jacobs, C., Domian, I. J., Maddock, J. R. & Shapiro, L. (1999). Cell cycledependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division. Cell 97, 111-120.
28. Jacobs, C., Hung, D. & Shapiro, L. (2001). Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. Proc Natl Acad Sci U S A 98, 4095-4100.
29. Jacobs, C., Ausmees, N., Cordwell, S. J., Shapiro, L. & Laub, M. T. (2003). Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol Microbiol 47, 1279-1290.
30. Jenal, U. (2009). The role of proteolysis in the Caulobacter crescentus cell cycle and development. Res Microbiol 160, 687-695.
31. Jonas, K., Chen, Y. E. & Laub, M. T. (2011). Modularity of the bacterial cell cycle enables independent spatial and temporal control of DNA replication. Curr Biol 21, 1092-1101.
32. Kahng, L. S. & Shapiro, L. (2001). The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J Bacteriol 183, 3065-3075.
33. Kelly, A. J., Sackett, M. J., Din, N., Quardokus, E. & Brun, Y. V. (1998). Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev 12, 880-893.
34. Kim, J., Heindl, J. E. & Fuqua, C. (2013). Coordination of division and development influences complex multicellular behavior in Agrobacterium tumefaciens. PLoS ONE 8, e56682.
35. Kobayashi, H., De Nisco, N. J., Chien, P., Simmons, L. A. & Walker, G. C. (2009). Sinorhizobium meliloti CpdR1 is critical for coordinating cell cycle progression and the symbiotic chronic infection. Mol Microbiol 73, 586-600.
36. Lam, H., Matroule, J. Y. & Jacobs-Wagner, C. (2003). The asymmetric spatial distribution of bacterial signal transduction proteins coordinates cell cycle events. Dev Cell 5, 149-159.
37. Latch, J. N. & Margolin, W. (1997). Generation of buds, swellings, and branches instead of filaments after blocking the cell cycle of Rhizobium meliloti. J Bacteriol 179, 2373-2381.
38. Laub, M. T., Chen, S. L., Shapiro, L. & McAdams, H. H. (2002). Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci U S A 99, 4632-4637.
39. Laub, M. T., Biondi, E. G. & Skerker, J. M. (2007). Phosphotransfer profiling: systematic mapping of two-component signal transduction pathways and phosphorelays. Methods Enzymol 423, 531-548.
40. Leigh, J. A., Signer, E. R. & Walker, G. C. (1985). Exopolysaccharidedeficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A 82, 6231-6235.
41. Levi, A. & Jenal, U. (2006). Holdfast formation in motile swarmer cells optimizes surface attachment during Caulobacter crescentus development. J Bacteriol 188, 5315-5318.
42. Matroule, J. Y., Lam, H., Burnette, D. T. & Jacobs-Wagner, C. (2004). Cytokinesis monitoring during development; rapid pole-to-pole shuttling of a signaling protein by localized kinase and phosphatase in Caulobacter. Cell 118, 579-590.
43. McAdams, H. H. & Shapiro, L. (2009). System-level design of bacterial cell cycle control. FEBS Lett 583, 3984-3991.
44. Mergaert, P., Uchiumi, T., Alunni, B., Evanno, G., Cheron, A., Catrice, O., Mausset, A. E., Barloy-Hubler, F., Galibert, F. & other authors (2006). Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci U S A 103, 5230-5235.
45. Quon, K. C., Marczynski, G. T. & Shapiro, L. (1996). Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84, 83-93.
46. Quon, K. C., Yang, B., Domian, I. J., Shapiro, L. & Marczynski, G. T. (1998). Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci U S A 95, 120-125.
47. Robertson, G. T., Reisenauer, A., Wright, R., Jensen, R. B., Jensen, A., Shapiro, L. & Roop, R. M., II (2000). The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182, 3482-3489.
48. Roop, R. M., II, Robertson, G. T., Ferguson, G. P., Milford, L. E., Winkler, M. E. & Walker, G. C. (2002). Seeking a niche: putative contributions of the hfq and bacA gene products to the successful adaptation of the brucellae to their intracellular home. Vet Microbiol 90, 349-363.
49. Sackett, M. J., Kelly, A. J. & Brun, Y. V. (1998). Ordered expression of ftsQA and ftsZ during the Caulobacter crescentus cell cycle. Mol Microbiol 28, 421-434.
50. Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G. & Puhler, A. (1994). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69-73.
51. Schroeder, B. K., House, B. L., Mortimer, M. W., Yurgel, S. N., Maloney, S. C., Ward, K. L. & Kahn, M. L. (2005). Development of a functional genomics platform for Sinorhizobium meliloti: construction of an ORFeome. Appl Environ Microbiol 71, 5858-5864.
52. Sibley, C. D., MacLellan, S. R. & Finan, T. (2006). The Sinorhizobium meliloti chromosomal origin of replication. Microbiology 152, 443-455.
53. Skerker, J. M. & Laub, M. T. (2004). Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2, 325-337.
54. Tsokos, C. G. & Laub, M. T. (2012). Polarity and cell fate asymmetry in Caulobacter crescentus. Curr Opin Microbiol 15, 744-750.
55. Tsokos, C. G., Perchuk, B. S. & Laub, M. T. (2011). A dynamic complex of signaling proteins uses polar localization to regulate cellfate asymmetry in Caulobacter crescentus. Dev Cell 20, 329-341.
56. Ugalde, R. A. (1999). Intracellular lifestyle of Brucella spp. Common genes with other animal pathogens, plant pathogens, and endosymbionts. Microbes Infect 1, 1211-1219.
57. Van de Velde, W., Zehirov, G., Szatmari, A., Debreczeny, M., Ishihara, H., Kevei, Z., Farkas, A., Mikulass, K., Nagy, A. & other authors (2010). Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122-1126.
58. Van der Henst, C., Beaufay, F., Mignolet, J., Didembourg, C., Colinet, J., Hallet, B., Letesson, J. J. & De Bolle, X. (2012). The histidine kinase PdhS controls cell cycle progression of the pathogenic alphaproteobacterium Brucella abortus. J Bacteriol 194, 5305-5314.
59. Viollier, P. H., Sternheim, N. & Shapiro, L. (2002). Identification of a localization factor for the polar positioning of bacterial structural and regulatory proteins. Proc Natl Acad Sci U S A 99, 13831-13836.
60. Wheeler, R. T. & Shapiro, L. (1999). Differential localization of two histidine kinases controlling bacterial cell differentiation. Mol Cell 4, 683-694.
61. Wortinger, M., Sackett, M. J. & Brun, Y. V. (2000). CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus. EMBO J 19, 4503-4512.
62. Wright, R., Stephens, C. & Shapiro, L. (1997). The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J Bacteriol 179, 5869-5877.
63. Wu, J., Ohta, N. & Newton, A. (1998). An essential, multicomponent signal transduction pathway required for cell cycle regulation in Caulobacter. Proc Natl Acad Sci U S A 95, 1443-1448.