ComGA-RelA interaction and persistence in the Bacillus subtilisK-state

Molecular Microbiology

Volumn 97, Issue 3, 2015, Pages 454-471

  Hahn, Jeanette ^a   Tanner, Andrew W ^a   Carabetta, Valerie J ^a   Cristea, Ileana M ^b   Dubnau, David ^a  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

(P)PPGPP; DNA BINDING PROTEIN; KANAMYCIN; OXOLINIC ACID; PROTEIN COMGA; RIBOSOME RNA; SYNTHETASE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; COMA PROTEIN, BACTERIA; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; GUANOSINE 3' DIPHOSPHATE 5' TRIPHOSPHATE; GUANOSINE 3',5'-POLYPHOSPHATE SYNTHETASES; LIGASE; PROTEIN BINDING;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACILLUS SUBTILIS; BACTERIUM TRANSFORMATION; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GROWTH INHIBITION; HYDROLYSIS; K STATE; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA SYNTHESIS; RNA TRANSCRIPTION; BIOSYNTHESIS; CELL DIVISION; GENE EXPRESSION REGULATION; GENETIC TRANSFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PROTEIN ANALYSIS;

BACILLUS SUBTILIS;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL DIVISION; DNA TRANSFORMATION COMPETENCE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GUANOSINE PENTAPHOSPHATE; GUANOSINE TETRAPHOSPHATE; LIGASES; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RNA, RIBOSOMAL;

EID: 84937970567     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13040     Document Type: Article

References (83)

1. Abbott, M., and McKinney, J. (2013) Understanding and Applying Research Design. Hoboken, NJ: John Wiley & Sons, Inc., p. xix. 425 pp.
2. Acar, M., Mettetal, J.T., and van Oudenaarden, A. (2008) Stochastic switching as a survival strategy in fluctuating environments. Nat Genet 40: 471-475.
3. Albano, M., Hahn, J., and Dubnau, D. (1987) Expression of competence genes in Bacillus subtilis. J Bacteriol 169: 3110-3117.
4. Amato, S.M., Orman, M.A., and Brynildsen, M.P. (2013) Metabolic control of persister formation in Escherichia coli. Mol Cell 50: 475-487.
5. Aviv, M., Giladi, H., Oppenheim, A.B., and Glaser, G. (1996) Analysis of the shut-off of ribosomal RNA promoters in Escherichia coli upon entering the stationary phase of growth. FEMS Microbiol Lett 140: 71-76.
6. Balaban, N.Q., Merrin, J., Chait, R., Kowalik, L., and Leibler, S. (2004) Bacterial persistence as a phenotypic switch. Science 305: 1622-1625.
7. Berka, R.M., Hahn, J., Albano, M., Draskovic, I., Persuh, M., Cui, X., etal. (2002) Microarray analysis of the Bacillus subtilis K-state: genome-wide expression changes dependent on ComK. Mol Microbiol 43: 1331-1345.
8. Biswas, G.D., Sox, T., and Sparling, P.F. (1977) Factors affecting genetic transformation of Neisseria gonorrhoeae. J Bacteriol 129: 983-992.
9. Briley, K., Jr, Dorsey-Oresto, A., Prepiak, P., Dias, M.J., Mann, J.M., and Dubnau, D. (2011a) The secretion ATPase ComGA is required for the binding and transport of transforming DNA. Mol Microbiol 81: 818-830.
10. Briley, K., Jr, Prepiak, P., Dias, M.J., Hahn, J., and Dubnau, D. (2011b) Maf acts downstream of ComGA to arrest cell division in competent cells of B.subtilis. Mol Microbiol 81: 23-39.
11. Brown, N.C. (1971) Inhibition of bacterial DNA replication by 6-(p-hydroxyphenylazo)-uracil: differential effect on repair and semi-conservative synthesis in Bacillus subtilis. J Mol Biol 59: 1-16.
12. Butler, Y.X., Abhayawardhane, Y., and Stewart, G.C. (1993) Amplification of the Bacillus subtilis maf gene results in arrested septum formation. J Bacteriol 175: 3139-3145.
13. Cao, M., Kobel, P.A., Morshedi, M.M., Wu, M.F., Paddon, C., and Helmann, J.D. (2002) Defining the Bacillus subtilis sigma(W) regulon: a comparative analysis of promoter consensus search, run-off transcription/macroarray analysis (ROMA), and transcriptional profiling approaches. J Mol Biol 316: 443-457.
14. Carabetta, V.J., Silhavy, T.J., and Cristea, I.M. (2010) The response regulator SprE (RssB) is required for maintaining poly(A) polymerase I-degradosome association during stationary phase. J Bacteriol 192: 3713-3721.
15. Carabetta, V.J., Tanner, A.W., Greco, T.M., Defrancesco, M., Cristea, I.M., and Dubnau, D. (2013) A complex of YlbF, YmcA and YaaT regulates sporulation, competence and biofilm formation by accelerating the phosphorylation of Spo0A. Mol Microbiol 88: 283-300.
16. Chung, Y.S., Breidt, F., and Dubnau, D. (1998) Cell surface localization and processing of the ComG proteins, required for DNA binding during transformation of Bacillus subtilis. Mol Microbiol 29: 905-913.
17. Cristea, I.M., Williams, R., Chait, B.T., and Rout, M.P. (2005) Fluorescent proteins as proteomic probes. Mol Cell Proteomics 4: 1933-1941.
18. Dagkessamanskaia, A., Moscoso, M., Henard, V., Guiral, S., Overweg, K., Reuter, M., etal. (2004) Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol Microbiol 51: 1071-1086.
19. Dahl, J.L., Kraus, C.N., Boshoff, H.I., Doan, B., Foley, K., Avarbock, D., etal. (2003) The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc Natl Acad Sci USA 100: 10026-10031.
20. Dalebroux, Z.D., and Swanson, M.S. (2012) ppGpp: magic beyond RNA polymerase. Nat Rev Microbiol 10: 203-212.
21. Fridman, O., Goldberg, A., Ronin, I., Shoresh, N., and Balaban, N.Q. (2014) Optimization of lag time underlies antibiotic tolerance in evolved bacterial populations. Nature 513: 418-421.
22. Gaca, A.O., Colomer-Winter, C., and Lemos, J.A. (2015) Many means to a common end: the intricacies of (p)ppGpp metabolism and Its control of bacterial homeostasis. J Bacteriol 197: 1146-1156.
23. Gralla, J.D. (2005) Escherichia coli ribosomal RNA transcription: regulatory roles for ppGpp, NTPs, architectural proteins and a polymerase-binding protein. Mol Microbiol 55: 973-977.
24. Greco, T.M., Miteva, Y., Conlon, F.L., and Cristea, I.M. (2012) Complementary proteomic analysis of protein complexes. Methods Mol Biol 917: 391-407.
25. Hahn, J., Maier, B., Haijema, B.J., Sheetz, M., and Dubnau, D. (2005) Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. Cell 122: 59-71.
26. Haijema, B.J., Hahn, J., Haynes, J., and Dubnau, D. (2001) A ComGA-dependent checkpoint limits growth during the escape from competence. Mol Microbiol 40: 52-64.
27. Hamoen, L.W., Smits, W.K., de Jong, A., Holsappel, S., and Kuipers, O.P. (2002) Improving the predictive value of the competence transcription factor (ComK) binding site in Bacillus subtilis using a genomic approach. Nucleic Acids Res 30: 5517-5528.
28. Hoa, T.T., Tortosa, P., Albano, M., and Dubnau, D. (2002) Rok (YkuW) regulates genetic competence in Bacillus subtilis by directly repressing comK. Mol Microbiol 43: 15-26.
29. Inaoka, T., and Ochi, K. (2002) RelA protein is involved in induction of genetic competence in certain Bacillus subtilis strains by moderating the level of intracellular GTP. J Bacteriol 184: 3923-3930.
30. Johnsen, P.J., Dubnau, D., and Levin, B.R. (2009) Episodic selection and the maintenance of competence and natural transformation in Bacillus subtilis. Genetics 181: 1521-1533.
31. Joshi, P., Greco, T.M., Guise, A.J., Luo, Y., Yu, F., Nesvizhskii, A.I., and Cristea, I.M. (2013) The functional interactome landscape of the human histone deacetylase family. Mol Syst Biol 9: 672.
32. Kearns, D.B., and Losick, R. (2005) Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev 19: 3083-3094.
33. Kim, C., Mwangi, M., Chung, M., Milheirico, C., de Lencastre, H., and Tomasz, A. (2013) The mechanism of heterogeneous beta-lactam resistance in MRSA: key role of the stringent stress response. PLoS ONE 8: e82814.
34. Korch, S.B., Henderson, T.A., and Hill, T.M. (2003) Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol Microbiol 50: 1199-1213.
35. Kramer, N., Hahn, J., and Dubnau, D. (2007) Multiple interactions among the competence proteins of Bacillus subtilis. Mol Microbiol 65: 454-464.
36. Kussell, E., and Leibler, S. (2005) Phenotypic diversity, population growth, and information in fluctuating environments. Science 309: 2075-2078.
37. Kussell, E., Kishony, R., Balaban, N.Q., and Leibler, S. (2005) Bacterial persistence: a model of survival in changing environments. Genetics 169: 1807-1814.
38. Kuwahara, H., and Soyer, O.S. (2012) Bistability in feedback circuits as a byproduct of evolution of evolvability. Mol Syst Biol 8: 564.
39. Leisner, M., Stingl, K., Radler, J.O., and Maier, B. (2007) Basal expression rate of comK sets a 'switching-window' into the K-state of Bacillus subtilis. Mol Microbiol 63: 1806-1816.
40. Lemon, K.P., and Grossman, A.D. (2000) Movement of replicating DNA through a stationary replisome. Mol Cell 6: 1321-1330.
41. Leung, V., and Levesque, C.M. (2012) A stress-inducible quorum-sensing peptide mediates the formation of persister cells with noninherited multidrug tolerance. J Bacteriol 194: 2265-2274.
42. Levy, S.F., Ziv, N., and Siegal, M.L. (2012) Bet hedging in yeast by heterogeneous, age-correlated expression of a stress protectant. PLoS Biol 10: e1001325.
43. Lindqvist, R. (2006) Estimation of Staphylococcus aureus growth parameters from turbidity data: characterization of strain variation and comparison of methods. Appl Environ Microbiol 72: 4862-4870.
44. Liu, K., Bittner, A.N., and Wang, J.D. (2015) Diversity in (p)ppGpp metabolism and effectors. Curr Opin Microbiol 24C: 72-79.
45. Lo Scrudato, M., and Blokesch, M. (2012) The regulatory network of natural competence and transformation of Vibrio cholerae. PLoS Genet 8: e1002778.
46. Lorenz, M.G., and Wackernagel, W. (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58: 563-602.
47. Maamar, H., Raj, A., and Dubnau, D. (2007) Noise in gene expression determines cell fate in Bacillus subtilis. Science 317: 526-529.
48. MacFadyen, L.P., Chen, D., Vo, H.C., Liao, D., Sinotte, R., and Redfield, R.J. (2001) Competence development by Haemophilus influenzae is regulated by the availability of nucleic acid precursors. Mol Microbiol 40: 700-707.
49. Magnusson, L.U., Farewell, A., and Nystrom, T. (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13: 236-242.
50. Maisonneuve, E., and Gerdes, K. (2014) Molecular mechanisms underlying bacterial persisters. Cell 157: 539-548.
51. Maisonneuve, E., Castro-Camargo, M., and Gerdes, K. (2013) p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154: 1140-1150.
52. Mann, J.M., Carabetta, V.J., Cristea, I.M., and Dubnau, D. (2013) Complex formation and processing of the minor transformation pilins of Bacillus subtilis. Mol Microbiol 90: 1201-1215.
53. Martin, B., Granadel, C., Campo, N., Henard, V., Prudhomme, M., and Claverys, J.P. (2010) Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae. Mol Microbiol 75: 1513-1528.
54. Mechold, U., Cashel, M., Steiner, K., Gentry, D., and Malke, H. (1996) Functional analysis of a relA/spoT gene homolog from Streptococcus equisimilis. J Bacteriol 178: 1401-1411.
55. Mirouze, N., Prepiak, P., and Dubnau, D. (2011) Fluctuations in spo0A transcription control rare developmental transitions in Bacillus subtilis. PLoS Genet 7: e1002048.
56. Mirouze, N., Desai, Y., Raj, A., and Dubnau, D. (2012) Spo0A∼P imposes a temporal gate for the bimodal expression of competence in Bacillus subtilis. PLoS Genet 8: e1002586.
57. Mwangi, M.M., Kim, C., Chung, M., Tsai, J., Vijayadamodar, G., Benitez, M., etal. (2013) Whole-genome sequencing reveals a link between beta-lactam resistance and synthetases of the alarmone (p)ppGpp in Staphylococcus aureus. Microb Drug Resist 19: 153-159.
58. Nanamiya, H., Kasai, K., Nozawa, A., Yun, C.S., Narisawa, T., Murakami, K., etal. (2008) Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol 67: 291-304.
59. Natori, Y., Tagami, K., Murakami, K., Yoshida, S., Tanigawa, O., Moh, Y., etal. (2009) Transcription activity of individual rrn operons in Bacillus subtilis mutants deficient in (p)ppGpp synthetase genes, relA, yjbM, and ywaC. J Bacteriol 191: 4555-4561.
60. Neiditch, M.B., and Hughson, F.M. (2007) The regulation of histidine sensor kinase complexes by quorum sensing signal molecules. Methods Enzymol 423: 250-263.
61. Nelder, J.A., and Wedderburn, R.W.M. (1972) Generalized linear models. J R Stat Soc Ser A Stat Soc 135: 370-384.
62. Nester, E.W., and Stocker, B.A.D. (1963) Biosynthetic latency in early stages of deoxyribonucleic acid transformation in Bacillus subtilis. J Bacteriol 86: 785-796.
63. Nguyen, D., Joshi-Datar, A., Lepine, F., Bauerle, E., Olakanmi, O., Beer, K., etal. (2011) Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334: 982-986.
64. Nowak, S., Neidhart, J., Szendro, I.G., and Krug, J. (2014) Multidimensional epistasis and the transitory advantage of sex. PLoS Comput Biol 10: e1003836.
65. Ogura, M., Yamaguchi, H., Kobayashi, K., Ogasawara, N., Fujita, Y., and Tanaka, T. (2002) Whole-genome analysis of genes regulated by the Bacillus subtilis competence transcription factor ComK. J Bacteriol 184: 2344-2351.
66. Paul, B.J., Ross, W., Gaal, T., and Gourse, R.L. (2004) rRNA transcription in Escherichia coli. Annu Rev Genet 38: 749-770.
67. Piir, K., Paier, A., Liiv, A., Tenson, T., and Maivali, U. (2011) Ribosome degradation in growing bacteria. EMBO Rep 12: 458-462.
68. Potrykus, K., and Cashel, M. (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62: 35-51.
69. Redfield, R.J. (1988) Evolution of bacterial transformation: is sex with dead cells ever better than no sex at all? Genetics 119: 213-221.
70. Redfield, R.J. (1993) Genes for breakfast: the have-your-cake-and-eat-it-too of bacterial transformation. J Hered 84: 400-404.
71. Redfield, R.J., Schrag, M.R., and Dean, A.M. (1997) The evolution of bacterial transformation: sex with poor relations. Genetics 146: 27-38.
72. Schaffner, D.W. (1998) Predictive food microbiology Gedanken experiment: why do microbial growth data require a transformation? Food Microbiol 15: 185-189.
73. Schagger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100kDa. Anal Biochem 166: 368-379.
74. Scheich, C., Kummel, D., Soumailakakis, D., Heinemann, U., and Bussow, K. (2007) Vectors for co-expression of an unrestricted number of proteins. Nucleic Acids Res 35: e43.
75. Srivatsan, A., and Wang, J.D. (2008) Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 11: 100-105.
76. Srivatsan, A., Han, Y., Peng, J., Tehranchi, A.K., Gibbs, R., Wang, J.D., and Chen, R. (2008) High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet 4: e1000139.
77. Strahl, H., and Hamoen, L.W. (2010) Membrane potential is important for bacterial cell division. Proc Natl Acad Sci USA 107: 12281-12286.
78. Sureka, K., Ghosh, B., Dasgupta, A., Basu, J., Kundu, M., and Bose, I. (2008) Positive feedback and noise activate the stringent response regulator Rel in Mycobacteria. PLoS ONE 3: e1771.
79. Süel, G.M., Kulkarni, R.P., Dworkin, J., Garcia-Ojalvo, J., and Elowitz, M.B. (2007) Tunability and noise dependence in differentiation dynamics. Science 315: 1716-1719.
80. Tchigvintsev, A., Tchigvintsev, D., Flick, R., Popovic, A., Dong, A., Xu, X., etal. (2013) Biochemical and structural studies of conserved Maf proteins revealed nucleotide pyrophosphatases with a preference for modified nucleotides. Chem Biol 20: 1386-1398.
81. Thattai, M., and van Oudenaarden, A. (2004) Stochastic gene expression in fluctuating environments. Genetics 167: 523-530.
82. Van Valen, L. (1973) A new evolutionary law. Evol Theory 1: 1-30.
83. Wang, J.D., Sanders, G.M., and Grossman, A.D. (2007) Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128: 865-875.