CodY, a pleiotropic regulator, influences multicellular behaviour and efficient production of virulence factors in Bacillus cereus

Environmental Microbiology

Volumn 14, Issue 8, 2012, Pages 2233-2246

  Lindbäck, Toril ^b   Mols, Maarten ^a   Basset, Coraline ^b   Granum, Per Einar ^b   Kuipers, Oscar P ^a,c   Kovács, Ákos T ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^c KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; VIRULENCE FACTOR;

ARTICLE; BACILLUS CEREUS; BIOFILM; BIOSYNTHESIS; DNA MICROARRAY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

BACILLUS CEREUS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE DELETION; TRANSCRIPTION FACTORS; TRANSCRIPTOME; VIRULENCE FACTORS;

BACILLUS CEREUS; BACILLUS CEREUS ATCC 14579; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); FIRMICUTES; HEXAPODA;

EID: 84864378360     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02766.x     Document Type: Article

References (73)

1. Abee, T., Kovacs, A.T., Kuipers, O.P., and van der Veen, S. (2011) Biofilm formation and dispersal in Gram-positive bacteria. Curr Opin Biotechnol 22: 172-179.
2. Arnaud, M., Chastanet, A., and Debarbouille, M. (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
3. Aronson, A.I., and Shai, Y. (2001) Why Bacillus thuringiensis insecticidal toxins are so effective: unique features of their mode of action. FEMS Microbiol Lett 195: 1-8.
4. Baldi, P., and Long, A.D. (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509-519.
5. Beecher, D.J., and Wong, A.C. (1994) Identification of hemolysin BL-producing Bacillus cereus isolates by a discontinuous hemolytic pattern in blood agar. Appl Environ Microbiol 60: 1646-1651.
6. Belitsky, B.R., and Sonenshein, A.L. (2008) Genetic and biochemical analysis of CodY-binding sites in Bacillus subtilis. J Bacteriol 190: 1224-1236.
7. Belitsky, B.R., and Sonenshein, A.L. (2011) Contributions of multiple binding sites and effector-independent binding to CodY-mediated regulation in Bacillus subtilis. J Bacteriol 193: 473-484.
8. Bennett, H.J., Pearce, D.M., Glenn, S., Taylor, C.M., Kuhn, M., Sonenshein, A.L., etal. (2007) Characterization of relA and codY mutants of Listeria monocytogenes: identification of the CodY regulon and its role in virulence. Mol Microbiol 63: 1453-1467.
9. Berg, G., Eberl, L., and Hartmann, A. (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7: 1673-1685.
10. Bergara, F., Ibarra, C., Iwamasa, J., Patarroyo, J.C., Aguilera, R., and Marquez-Magana, L.M. (2003) CodY is a nutritional repressor of flagellar gene expression in Bacillus subtilis. J Bacteriol 185: 3118-3126.
11. Bottone, E.J. (2010) Bacillus cereus, a volatile human pathogen. Clin Microbiol Rev 23: 382-398.
12. Branda, S.S., Chu, F., Kearns, D.B., Losick, R., and Kolter, R. (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59: 1229-1238.
13. Callegan, M.C., Kane, S.T., Cochran, D.C., Novosad, B., Gilmore, M.S., Gominet, M., and Lereclus, D. (2005) Bacillus endophthalmitis: roles of bacterial toxins and motility during infection. Invest Ophthalmol Vis Sci 46: 3233-3238.
14. Di Franco, C., Beccari, E., Santini, T., Pisaneschi, G., and Tecce, G. (2002) Colony shape as a genetic trait in the pattern-forming Bacillus mycoides. BMC Microbiol 2: 33.
15. Dietrich, R., Fella, C., Strich, S., and Martlbauer, E. (1999) Production and characterization of monoclonal antibodies against the hemolysin BL enterotoxin complex produced by Bacillus cereus. Appl Environ Microbiol 65: 4470-4474.
16. Dietrich, R., Moravek, M., Burk, C., Granum, P.E., and Martlbauer, E. (2005) Production and characterization of antibodies against each of the three subunits of the Bacillus cereus nonhemolytic enterotoxin complex. Appl Environ Microbiol 71: 8214-8220.
17. Dineen, S.S., Villapakkam, A.C., Nordman, J.T., and Sonenshein, A.L. (2007) Repression of Clostridium difficile toxin gene expression by CodY. Mol Microbiol 66: 206-219.
18. Dunn, A.K., and Handelsman, J. (1999) A vector for promoter trapping in Bacillus cereus. Gene 226: 297-305.
19. Fagerlund, A., Ween, O., Lund, T., Hardy, S.P., and Granum, P.E. (2004) Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiology 150: 2689-2697.
20. Fisher, S.H. (1999) Regulation of nitrogen metabolism in Bacillus subtilis: vive la difference! Mol Microbiol 32: 223-232.
21. Foster, R.C. (1988) Microenvironments of soil microorganisms. Biol Fertil Soils 6: 189-203.
22. Garbeva, P., van Veen, J.A., and van Elsas, J.D. (2003) Predominant Bacillus spp. in agricultural soil under different management regimes detected via PCR-DGGE. Microb Ecol 45: 302-316.
23. Ghosh, A.C. (1978) Prevalence of Bacillus cereus in the faeces of healthy adults. J Hyg (Lond) 80: 233-236.
24. Gohar, M., Faegri, K., Perchat, S., Ravnum, S., Okstad, O.A., Gominet, M., etal. (2008) The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3: e2793.
25. Grande Burgos, M.J., Kovacs, A.T., Mironczuk, A.M., Abriouel, H., Galvez, A., and Kuipers, O.P. (2009) Response of Bacillus cereus ATCC 14579 to challenges with sublethal concentrations of enterocin AS-48. BMC Microbiol 9: 227.
26. Guedon, E., Sperandio, B., Pons, N., Ehrlich, S.D., and Renault, P. (2005) Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151: 3895-3909.
27. Harlow, E., and Lane, D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory.
28. Helgason, E., Okstad, O.A., Caugant, D.A., Johansen, H.A., Fouet, A., Mock, M., etal. (2000) Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis - one species on the basis of genetic evidence. Appl Environ Microbiol 66: 2627-2630.
29. Hendriksen, W.T., Bootsma, H.J., Estevao, S., Hoogenboezem, T., de Jong, A., de Groot, R., etal. (2008) CodY of Streptococcus pneumoniae: link between nutritional gene regulation and colonization. J Bacteriol 190: 590-601.
30. den Hengst, C.D., van Hijum, S.A., Geurts, J.M., Nauta, A., Kok, J., and Kuipers, O.P. (2005) The Lactococcus lactis CodY regulon: identification of a conserved cis-regulatory element. J Biol Chem 280: 34332-34342.
31. van Hijum, S.A., de Jong, A., Buist, G., Kok, J., and Kuipers, O.P. (2003a) UniFrag and GenomePrimer: selection of primers for genome-wide production of unique amplicons. Bioinformatics 19: 1580-1582.
32. van Hijum, S.A., Garcia de la Nava, J., Trelles, O., Kok, J., and Kuipers, O.P. (2003b) MicroPreP: a cDNA microarray data pre-processing framework. Appl Bioinformatics 2: 241-244.
33. van Hijum, S.A., de Jong, A., Baerends, R.J., Karsens, H.A., Kramer, N.E., Larsen, R., etal. (2005) A generally applicable validation scheme for the assessment of factors involved in reproducibility and quality of DNA-microarray data. BMC Genomics 6: 77.
34. Houry, A., Briandet, R., Aymerich, S., and Gohar, M. (2010) Involvement of motility and flagella in Bacillus cereus biofilm formation. Microbiology 156: 1009-1018.
35. Hsueh, Y.H., Somers, E.B., Lereclus, D., and Wong, A.C. (2006) Biofilm formation by Bacillus cereus is influenced by PlcR, a pleiotropic regulator. Appl Environ Microbiol 72: 5089-5092.
36. Hsueh, Y.H., Somers, E.B., and Wong, A.C. (2008) Characterization of the codY gene and its influence on biofilm formation in Bacillus cereus. Arch Microbiol 189: 557-568.
37. Ivanova, N., Sorokin, A., Anderson, I., Galleron, N., Candelon, B., Kapatral, V., etal. (2003) Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423: 87-91.
38. Janes, B.K., and Stibitz, S. (2006) Routine markerless gene replacement in Bacillus anthracis. Infect Immun 74: 1949-1953.
39. Jensen, G.B., Hansen, B.M., Eilenberg, J., and Mahillon, J. (2003) The hidden lifestyles of Bacillus cereus and relatives. Environ Microbiol 5: 631-640.
40. Joseph, P., Ratnayake-Lecamwasam, M., and Sonenshein, A.L. (2005) A region of Bacillus subtilis CodY protein required for interaction with DNA. J Bacteriol 187: 4127-4139.
41. 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.
42. Kim, H.J., Kim, S.I., Ratnayake-Lecamwasam, M., Tachikawa, K., Sonenshein, A.L., and Strauch, M. (2003) Complex regulation of the Bacillus subtilis aconitase gene. J Bacteriol 185: 1672-1680.
43. Kobayashi, K. (2007) Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol 189: 4920-4931.
44. Kolsto, A.B., Tourasse, N.J., and Okstad, O.A. (2009) What sets Bacillus anthracis apart from other Bacillus species? Annu Rev Microbiol 63: 451-476.
45. Kuipers, O.P., de Jong, A., Baerends, R.J., van Hijum, S.A., Zomer, A.L., Karsens, H.A., etal. (2002) Transcriptome analysis and related databases of Lactococcus lactis. Antonie Van Leeuwenhoek 82: 113-122.
46. Lechner, S., Mayr, R., Francis, K.P., Pruss, B.M., Kaplan, T., Wiessner-Gunkel, E., etal. (1998) Bacillus weihenstephanensis sp. nov. is a new psychrotolerant species of the Bacillus cereus group. Int J Syst Bacteriol 48 (Part 4): 1373-1382.
47. Lemos, J.A., Nascimento, M.M., Lin, V.K., Abranches, J., and Burne, R.A. (2008) Global regulation by (p)ppGpp and CodY in Streptococcus mutans. J Bacteriol 190: 5291-5299.
48. Levdikov, V.M., Blagova, E., Joseph, P., Sonenshein, A.L., and Wilkinson, A.J. (2006) The structure of CodY, a GTP- and isoleucine-responsive regulator of stationary phase and virulence in gram-positive bacteria. J Biol Chem 281: 11366-11373.
49. Lindbäck, T., and Granum, P.E. (2006) Detection and purification of Bacillus cereus enterotoxins. In Methods in Biotechnology, Food-Borne Pathogens: Methods and Protocols. Adley, C.C. (ed.). Totowa, NJ, USA: Humana Press, pp. 15-26.
50. Livak, K.J., and Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
51. Mahillon, J., Chungjatupornchai, W., Decock, J., Dierickx, S., Michiels, F., Peferoen, M., and Joos, H. (1989) Transformation of Bacillus thuringiensis by electroporation. FEMS Microbiol Lett 60: 205-210.
52. Majerczyk, C.D., Sadykov, M.R., Luong, T.T., Lee, C., Somerville, G.A., and Sonenshein, A.L. (2008) Staphylococcus aureus CodY negatively regulates virulence gene expression. J Bacteriol 190: 2257-2265.
53. Malke, H., and Ferretti, J.J. (2007) CodY-affected transcriptional gene expression of Streptococcus pyogenes during growth in human blood. J Med Microbiol 56: 707-714.
54. Marraffini, L.A., and Schneewind, O. (2006) Targeting proteins to the cell wall of sporulating Bacillus anthracis. Mol Microbiol 62: 1402-1417.
55. Mock, M., and Fouet, A. (2001) Anthrax. Annu Rev Microbiol 55: 647-671.
56. Molle, V., Nakaura, Y., Shivers, R.P., Yamaguchi, H., Losick, R., Fujita, Y., and Sonenshein, A.L. (2003) Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol 185: 1911-1922.
57. Mols, M., de Been, M., Zwietering, M.H., Moezelaar, R., and Abee, T. (2007) Metabolic capacity of Bacillus cereus strains ATCC 14579 and ATCC 10987 interlinked with comparative genomics. Environ Microbiol 9: 2933-2944.
58. Nakamura, L.K. (1998) Bacillus pseudomycoides sp. nov. Int J Syst Bacteriol 48 (Part 3): 1031-1035.
59. Ratnayake-Lecamwasam, M., Serror, P., Wong, K.W., and Sonenshein, A.L. (2001) Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev 15: 1093-1103.
60. Romero, D., Vlamakis, H., Losick, R., and Kolter, R. (2011) An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol 80: 1155-1168.
61. Rosenquist, H., Smidt, L., Andersen, S.R., Jensen, G.B., and Wilcks, A. (2005) Occurrence and significance of Bacillus cereus and Bacillus thuringiensis in ready-to-eat food. FEMS Microbiol Lett 250: 129-136.
62. van Schaik, W., Chateau, A., Dillies, M.A., Coppee, J.Y., Sonenshein, A.L., and Fouet, A. (2009) The global regulator CodY regulates toxin gene expression in Bacillus anthracis and is required for full virulence. Infect Immun 77: 4437-4445.
63. Serror, P., and Sonenshein, A.L. (1996) CodY is required for nutritional repression of Bacillus subtilis genetic competence. J Bacteriol 178: 5910-5915.
64. Silo-Suh, L.A., Lethbridge, B.J., Raffel, S.J., He, H., Clardy, J., and Handelsman, J. (1994) Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl Environ Microbiol 60: 2023-2030.
65. Slack, F.J., Serror, P., Joyce, E., and Sonenshein, A.L. (1995) A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon. Mol Microbiol 15: 689-702.
66. Sonenshein, A.L. (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8: 203-207.
67. Sonenshein, A.L. (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5: 917-927.
68. Stabb, E.V., Jacobson, L.M., and Handelsman, J. (1994) Zwittermicin A-producing strains of Bacillus cereus from diverse soils. Appl Environ Microbiol 60: 4404-4412.
69. Stenfors Arnesen, L.P., Fagerlund, A., and Granum, P.E. (2008) From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 32: 579-606.
70. Stenz, L., Francois, P., Whiteson, K., Wolz, C., Linder, P., and Schrenzel, J. (2011) The CodY pleiotropic repressor controls virulence in Gram-positive pathogens. FEMS Immunol Med Microbiol 62: 123-139.
71. von Stetten, F., Mayr, R., and Scherer, S. (1999) Climatic influence on mesophilic Bacillus cereus and psychrotolerant Bacillus weihenstephanensis populations in tropical, temperate and alpine soil. Environ Microbiol 1: 503-515.
72. Vilain, S., Luo, Y., Hildreth, M.B., and Brozel, V.S. (2006) Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Appl Environ Microbiol 72: 4970-4977.
73. Wray, L.V., Jr, Ferson, A.E., and Fisher, S.H. (1997) Expression of the Bacillus subtilis ureABC operon is controlled by multiple regulatory factors including CodY, GlnR, TnrA, and Spo0H. J Bacteriol 179: 5494-5501.