Small RNAs of pseudomonas spp.

Pseudomonas

Volumn 6, Issue , 2006, Pages 3-28

  Sonnleitner, Elisabeth ^a   González, Nicolas ^b   Haas, Dieter ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

GacA; Post transcriptional regulation; Pseudomonas; RNA binding protein; Small RNA

Indexed keywords

EID: 84920076262     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-90-481-3909-5_1     Document Type: Chapter

References (95)

1. Wassarman, K.M., Zhang, A. and Storz, G. (1999) Small RNAs in Escherichia coli. Trends Microbiol. 7: 37-45.
2. Waters, L.S. and Storz, G. (2009) Regulatory RNAs in bacteria. Cell 136: 615-628.
3. Livny, J. and Waldor, M.K. (2007) Identification of small RNAs in diverse bacterial species. Curr. Opin. Microbiol. 10: 96-101.
4. Pichon, C. and Felden, B. (2007) Proteins that interact with bacterial small RNA regulators. FEMS Microbiol. Rev. 31: 614-625.
5. Majdalani, N., Vanderpool, C.K. and Gottesman, S. (2005) Bacterial small RNA regulators. Crit. Rev. Biochem. Mol. Biol. 40: 93-113.
6. Valentin-Hansen, P., Johansen, J. and Rasmussen, A.A. (2007) Small RNAs controlling outer membrane porins. Curr. Opin. Microbiol. 10: 152-155.
7. Valverde, C. and Haas, D. (2008) Small RNAs controlled by two-component systems, pp. 54-79. In R. Utsumi (ed.), Bacterial signal transduction: network and drug targets, Landes Bioscience. Austin, Texas, USA.
8. Altuvia, S. (2007) Identification of bacterial small non-coding RNAs: experimental approaches. Curr. Opin. Microbiol. 10: 257-261.
9. Vogel, J. and Wagner, E.G. (2007) Target identification of small noncoding RNAs in bacteria. Curr. Opin. Microbiol. 10: 262-270.
10. Tjaden, B., Saxena, R.M., Stolyar, S., Haynor, D.R., Kolker, E. and Rosenow, C. (2002) Transcriptome analysis of Escherichia coli using high-density oligonucleotide probe arrays. Nucleic Acids Res. 30: 3732-3738.
11. Vogel, J., Bartels, V., Tang, T.H., Churakov, G., Slagter-Jäger, J.G., Hüttenhofer, A. and Wagner, E.G. (2003) RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res. 31: 6435-6443.
12. Barrick, J.E., Sudarsan, N., Weinberg, Z., Ruzzo, W.L. and Breaker, R.R. (2005) 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 11: 774-784.
13. Wilderman, P.J., Sowa, N.A., FitzGerald, D.J., FitzGerald, P.C., Gottesman, S., Ochsner, U.A. and Vasil, M.L. (2004) Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc. Natl. Acad. Sci. USA 101: 9792-9797.
14. Livny, J., Brencic, A., Lory, S. and Waldor, M.K. (2006) Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2. Nucleic Acids Res. 34: 3484-3493.
15. González, N., Heeb, S., Valverde, C., Kay, E., Reimmann, C., Junier, T. and Haas, D. (2008) Genome-wide search reveals a novel GacA-regulated small RNA in Pseudomonas species. BMC Genomics 9: 167.
16. Sonnleitner, E., Sorger-Domenigg, T., Madej, M.J., Findeiss, S., Hackermüller, J., Hüttenhofer, A., Stadler, P.F., Bläsi, U. and Moll, I. (2008) Detection of small RNAs in Pseudomonas aeruginosa by RNomics and structure-based bioinformatic tools. Microbiology 154: 3175-3187.
17. Kay, E., Humair, B., Dénervaud, V., Riedel, K., Spahr, S., Eberl, L., Valverde., C. and Haas, D. (2006) Two GacA-dependent small RNAs modulate the quorum sensing response in Pseudomonas aeruginosa. J. Bacteriol. 188: 6026-6033.
18. Toschka, H.Y., Struck, J.C. and Erdmann, V.A. (1989) The 4.5S RNA gene from Pseudomonas aeruginosa. Nucleic Acids Res. 17: 31-36.
19. Heurlier, K., Williams, F., Heeb, S., Dormond, C., Pessi, G., Singer, D., Cámara, M., Williams, P. and Haas, D. (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J. Bacteriol. 186: 2936-2945.
20. Vogel, D.W., Hartmann, R.K., Struck, J.C., Ulbrich, N. and Erdmann, V.A. (1987) The sequence of the 6S RNA gene of Pseudomonas aeruginosa. Nucleic Acids Res. 15: 4583-4591.
21. Komine, Y., Kitabatake, M., Yokogawa, T., Nishikawa, K. and Inokuchi, H. (1994) A tRNAlike structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc. Natl. Acad. Sci. USA 91: 9223-9227.
22. Williams, K.P. and Bartel, D.P. (1996) Phylogenetic analysis of tmRNA secondary structure. RNA 2: 1306-1310.
23. Rivas, E. and Eddy, S.R. (2001) Noncoding RNA gene detection using comparative sequence analysis. BMC Bioinformatics 2: 8.
24. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., Brinkman, F.S., Hufnagle, W.O., Kowalik, D.J., Lagrou, M., Garber, R.L., Goltry, L., Tolentino, E., Westbrock-Wadman, S., Yuan, Y., Brody, L.L., Coulter, S.N., Folger, K.R., Kas, A., Larbig, K., Lim, R., Smith, K., Spencer, D., Wong, G.K., Wu, Z., Paulsen, I.T., Reizer, J., Saier, M.H., Hancock, R.E., Lory, S. and Olson, M.V. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
25. James, B.D., Olsen, G.J., Liu, J.S. and Pace, N.R. (1988) The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme. Cell 52: 19-26.
26. Valverde, C., Heeb, S., Keel, C. and Haas, D. (2003) RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol. Microbiol. 50: 1361-1379.
27. Heeb, S., Blumer, C. and Haas, D. (2002) Regulatory RNA as mediator in GacA/RsmAdependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J. Bacteriol. 184: 1046-1056.
28. Kay, E., Dubuis, C. and Haas, D. (2005) Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc. Natl. Acad. Sci. USA 102: 17136-17141.
29. Rowley, K.B., Clements, D.E., Mandel, M., Humphreys, T. and Patil, S.S. (1993) Multiple copies of a DNA sequence from Pseudomonas syringae pathovar phaseolicola abolish thermoregulation of phaseolotoxin production. Mol. Microbiol. 8: 625-635.
30. Aarons, S., Abbas, A., Adams, C., Fenton, A. and O'Gara, F. (2000) A regulatory RNA (PrrB RNA) modulates expression of secondary metabolite genes in Pseudomonas fluorescens F113. J. Bacteriol. 182: 3913-3919.
31. Trotochaud, A.E. and Wassarman, K.M. (2005) A highly conserved 6S RNA structure is required for regulation of transcription. Nat. Struct. Mol. Biol. 12: 313-319.
32. Kulkarni, P.R., Cui, X., Williams, J.W., Stevens, A.M. and Kulkarni, R.V. (2006) Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri. Nucleic Acids Res. 34: 3361-3369.
33. Wassarman, K.M. and Saecker, R.M. (2006) Synthesis-mediated release of a small RNA inhibitor of RNA polymerase. Science 314: 1601-1603.
34. Wassarman, K.M. (2007) 6S RNA: A regulator of transcription. Mol. Microbiol. 65: 1425-1431.
35. Keenan, R.J., Freymann, D.M., Stroud, R.M. and Walter, P. (2001) The signal recognition particle. Annu. Rev. Biochem. 70: 755-775.
36. Regalia, M., Rosenblad, M.A. and Samuelsson, T. (2002) Prediction of signal recognition particle RNA genes. Nucleic Acids Res. 30: 3368-3377.
37. Keiler, K.C. (2007) Physiology of tmRNA: What gets tagged and why? Curr. Opin. Microbiol. 10: 169-175.
38. Frank, D.N. and Pace, N.R. (1998) Ribonuclease P: unity and diversity in a tRNA processing ribozyme. Annu. Rev. Biochem. 67: 153-180.
39. Li, Y. and Altman, S. (2004) In search of RNase P RNA from microbial genomes. RNA 10: 1533-1540.
40. Drew, R. and Haq, M. (2004) Lessons from the ami operon, pp. 425-449. In J.-L. Ramos (ed.), Pseudomonas, Volume 2, Virulence and gene regulation. Kluwer Academic/Plenum Publishers, New York, USA.
41. Norman, R.A., Poh, C.L., Pearl, L.H., O'Hara, B.P. and Drew, R.E. (2000) Steric hindrance regulation of the Pseudomonas aeruginosa amidase operon. J. Biol. Chem. 275: 30660-30667.
42. Gelfand, M.S., Mironov, A.A., Jomantas, J., Kozlov, Y.I. and Perumov, D.A. (1999) A conserved RNA structure element involved in the regulation of bacterial riboflavin synthesis genes. Trends Genet. 15: 439-442.
43. Heeb, S., Heurlier, K., Valverde, C., Cámara, M., Haas, D. and Williams, P. (2004) Posttranscriptional regulation in Pseudomonas spp. via the Gac/Rsm regulatory network, pp. 239-255. In J.-L. Ramos (ed.), Pseudomonas, Volume 2, Virulence and gene regulation. Kluwer Academic/Plenum Publishers, New York, USA.
44. Lazdunski, A.M., Ventre, I. and Bleves, S. (2007) Cell-cell communication: quorum sensing and regulatory circuits in Pseudomonas aeruginosa, pp. 279-310. In J.-L. Ramos and A. Filloux (ed.), Pseudomonas, Volume 5, A model system in biology. Springer, London .
45. Ventre, I., Goodman, A.L., Filloux, A. and Lory, S. (2007) Modulation of bacterial lifestyles via two-component regulatory networks, pp. 311-340. In J.-L. Ramos and A. Filloux (ed.), Pseudomonas, Volume 5, A model system in biology. Springer, London.
46. Diggle, S.P., Cornelis, P., Williams, P. and Cámara, M. (2006) 4-quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int. J. Med. Microbiol. 296: 83-91.
47. Juhas, M., Eberl, L. and Tümmler, B. (2005) Quorum sensing: The power of cooperation in the world of Pseudomonas. Environ. Microbiol. 7: 459-471.
48. Gallagher, L.A. and Manoil, C. (2001) Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J. Bacteriol. 183: 6207-6214.
49. Rahme, L.G., Ausubel, F.M., Cao, H., Drenkard, E., Goumnerov, B.C., Lau, G.W., Mahajan- Miklos, S., Plotnikova, J., Tan, M.W., Tsongalis, J., Walendziewicz, C.L. and Tompkins, R.G. (2000) Plants and animals share functionally common bacterial virulence factors. Proc. Natl. Acad. Sci. USA 97: 8815-8821.
50. Goodman, A.L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R.S. and Lory, S. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7: 745-754.
51. Goodman, A.L., Merighi, M., Hyodo, M., Ventre, I., Filloux, A. and Lory, S. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev. 23: 249-259.
52. Ventre, I., Goodman, A.L., Valley-Gely, I., Vasseur, P., Soscia, C., Molin, S., Bleves, S., Lazdunski, A., Lory, S. and Filloux, A. (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl. Acad. Sci. USA 103: 171-176.
53. Laskowski, M.A. and Kazmierczak, B.I. (2006) Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infect. Immun. 74: 4462-4473.
54. Zolfaghar, I., Evans, D.J., Ronaghi, R. and Fleiszig, S.M. (2006) Type III secretion-dependent modulation of innate immunity as one of multiple factors regulated by Pseudomonas aeruginosa RetS. Infect. Immun. 74: 3880-3889.
55. Humair, B., González, N., Mossialos, D., Reimmann, C. and Haas, D. (2009) Temperatureresponsive sensing regulates biocontrol factor expression in Pseudomonas fluorescens CHA0. ISME J. 3: 955-965.
56. Workentine, M.-L., Chang, L., Ceri, H. and Turner, R.J. (2009) The GacS-GacA twocomponent regulatory system of Pseudomonas fluorescens: A bacterial two-hybrid analysis. FEMS Microbiol. Lett. 292: 50-56.
57. Dubuis, C., Keel, C. and Haas, D. (2007) Dialogues of root-colonizing biocontrol pseudomonads. Eur. J. Plant Pathol. 119: 311-328.
58. Heeb, S., Kuehne, S.A., Bycroft, M., Crivii, S., Allen, M.D., Haas, D., Cámara, M. and Williams, P. (2006) Functional analysis of the post-transcriptional regulator RsmA reveals a novel RNA-binding site. J. Mol. Biol. 355: 1026-1036.
59. Pessi, G., Williams, F., Hindle, Z., Heurlier, K., Holden, M.T., Cámara, M., Haas, D. and Williams, P. (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J. Bacteriol. 183: 6676-6683.
60. Babitzke, P. and Romeo, T. (2007) CsrB sRNA family: Sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol. 10: 156-163.
61. Sonnleitner, E., Schuster, M., Sorger-Domenigg, T., Greenberg, E.P. and Bläsi, U. (2006) Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa. Mol. Microbiol. 59: 1542-1558.
62. Sorger-Domenigg, T., Sonnleitner, E., Kaberdin, V.R. and Bläsi, U. (2007) Distinct and overlapping binding sites of Pseudomonas aeruginosa Hfq and RsmA proteins on the non-coding RNA RsmY. Biochem. Biophys. Res. Commun. 352: 769-773.
63. Reimmann, C., Beyeler, M., Latifi, A., Winteler, H., Foglino, M., Lazdunski, A. and Haas, D. (1997) The global activator GacA of Pseudomonas aeruginosa PAO1 positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol. Microbiol. 24: 309-319.
64. Pessi, G. and Haas, D. (2001) Dual control of hydrogen cyanide biosynthesis by the global activator GacA in Pseudomonas aeruginosa PAO1. FEMS Microbiol. Lett. 200: 73-78.
65. Lapouge, K., Schubert, M., Allain, F.H.T. and Haas, D. (2008) Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67: 241-253.
66. Haas, D. and Défago, G. (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3: 307-319.
67. Heeb, S. and Haas, D. (2001) Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. Mol. Plant-Microbe. Interact. 14: 1351-1363.
68. Laville, J., Voisard, C., Keel, C., Maurhofer, M., Défago, G. and Haas, D. (1992) Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proc. Natl. Acad. Sci. USA 89: 1562-1566.
69. Zuber, S., Carruthers, F., Keel, C., Mattart, A., Blumer, C., Pessi, G., Gigot-Bonnefoy, C., Schnider-Keel, U., Heeb, S., Reimmann, C. and Haas, D. (2003) GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. Mol. Plant. Microbe. Interact. 16: 634-644.
70. Reimmann, C., Valverde, C., Kay, E. and Haas, D. (2005) Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. J. Bacteriol. 187: 276-285.
71. Blumer, C., Heeb, S., Pessi, G. and Haas, D. (1999) Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc. Natl. Acad. Sci. USA 96: 14073-14078.
72. Heeb, S., Valverde, C., Gigot-Bonnefoy, C. and Haas, D. (2005) Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS Microbiol. Lett. 243: 251-258.
73. Chatterjee, A., Cui, Y., Yang, H., Collmer, A., Alfano, J.R. and Chatterjee, A.K. (2003) GacA, the response regulator of a two-component system, acts as a master regulator in Pseudomonas syringae pv. tomato DC3000 by controlling regulatory RNA, transcriptional activators, and alternate sigma factors. Mol. Plant. Microbe. Interact. 16: 1106-1117.
74. Valverde, C., Lindell, M., Wagner, E.G. and Haas, D. (2004) A repeated GGA motif is critical for the activity and stability of the riboregulator RsmY of Pseudomonas fluorescens. J. Biol. Chem. 279: 25066-25074.
75. Valverde, C. (2009) Artificial sRNAs activating the Gac/Rsm signal transduction pathway in Pseudomonas fluorescens. Arch. Microbiol. 191: 349-359.
76. Dubey, A.K., Baker, C.S., Romeo, T. and Babitzke, P. (2005) RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11: 1579-1587.
77. Lapouge, K., Sineva, E., Lindell, M., Starke, K., Baker, C.S., Babitzke, P. and Haas, D. (2007) Mechanism of hcnA mRNA recognition in the Gac/Rsm signal transduction pathway of Pseudomonas fluorescens. Mol. Microbiol. 66: 341-356.
78. Schubert, M., Lapouge, K., Duss, O., Oberstrass, F.C., Jelesarov, I., Haas, D. and Allain, F.H. (2007) Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA. Nat. Struct. Mol. Biol. 14: 807-813.
79. Vasil, M.L. (2007) How we learnt about iron acquisition in Pseudomonas aeruginosa: A series of very fortunate events. Biometals 20: 587-601.
80. Visca, P. (2004) Iron regulation and siderophore signalling in virulence by Pseudomonas aeruginosa, pp. 69-123. In J.-L. Ramos (ed.), Pseudomonas, Volume 2, Virulence and gene regulation. Springer, London.
81. Gaballa, A., Antelmann, H., Aguilar, C., Khakh, S.K., Song, K.B., Smaldone, G.T. and Helmann, J.D. (2008) The Bacillus subtilis iron-sparing response is mediated by a Furregulated small RNA and three small, basic proteins. Proc. Natl. Acad. Sci. USA 105: 11927-11932.
82. Massé, E. and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. USA 99: 4620-4625.
83. Bronstein, P.A., Filiatrault, M.J., Myers, C.R., Rutzke, M., Schneider, D.J. and Cartinhour, S.W. (2008) Global transcriptional responses of Pseudomonas syringae DC3000 to changes in iron bioavailability in vitro. BMC Microbiol. 8: 209.
84. Oglesby, A.G., Farrow, J.M. 3rd, Lee, J.H., Tomaras, A.P., Greenberg, E.P., Pesci, E.C. and Vasil, M.L. (2008) The influence of iron on Pseudomonas aeruginosa physiology: A regulatory link between iron and quorum sensing. J. Biol. Chem. 283: 15558-15567.
85. Haas, D., Gamper, M. and Zimmermann, A. (1992) Anaerobic control in Pseudomonas aeruginosa, pp. 177-187. In E. Galli, S. Silver and B. Witholt (ed.), Pseudomonas, molecular biology and biotechnology. American Society for Microbiology, Washington, D.C.
86. Thomas, K.L., Lloyd, D. and Boddy, L. (1994) Effects of oxygen, pH and nitrate concentration on denitrification by Pseudomonas species. FEMS Microbiol. Lett. 118: 181-186.
87. Alvarez-Ortega, C. and Harwood, C.S. (2007) Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol. Microbiol. 65: 153-165.
88. Sabra, W., Kim, E.J. and Zeng, A.P. (2002) Physiological responses of Pseudomonas aeruginosa PAO1 to oxidative stress in controlled microaerobic and aerobic cultures. Microbiology 148: 3195-3202.
89. Zimmermann, A., Reimmann, C., Galimand, M. and Haas, D. (1991) Anaerobic growth and cyanide synthesis of Pseudomonas aeruginosa depend on anr, a regulatory gene homologous with fnr of Escherichia coli. Mol. Microbiol. 5: 1483-1490.
90. Comolli, J.C. and Donohue, T.J. (2004) Differences in two Pseudomonas aeruginosa cbb3 cytochrome oxidases. Mol. Microbiol. 51: 1193-1203.
91. Ugidos, A., Morales, G., Rial, E., Williams, H.D. and Rojo, F. (2008) The coordinate regulation of multiple terminal oxidases by the Pseudomonas putida ANR global regulator. Environ. Microbiol. 10: 1690-1702.
92. Ye, R.W., Haas, D., Ka, J.-O., Krishnapillai, V., Zimmermann, A., Baird, C. and Tiedje, J.M. (1995) Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. J. Bacteriol. 177: 3606-3609.
93. Winteler, H.V. and Haas, D. (1996) The homologous regulators ANR of Pseudomonas aeruginosa and FNR of Escherichia coli have overlapping but distinct specificities for anaerobically inducible promoters. Microbiology 142: 685-693.
94. Toyofuku, M., Nomura, N., Kuno, E., Tashiro, Y., Nakajima, T. and Uchiyama, H.J. (2008) Influence of the Pseudomonas quinolone signal on denitrification in Pseudomonas aeruginosa. J. Bacteriol. 190: 7947-7956.
95. Hemm, M.R., Paul, B.J., Schneider, T.D., Storz, G. and Rudd, K.E. (2008) Small membrane proteins found by comparative genomics and ribosome binding site models. Mol. Microbiol. 70: 1487-1501.