Biosynthesis of carbapenem antibiotic and prodigiosin pigment in Serratia is under quorum sensing control

Molecular Microbiology

Volumn 36, Issue 3, 2000, Pages 539-556

  Thomson, N R ^a   Crow, M A ^a   McGowan, S J ^a   Cox, A ^a   Salmond, G P C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBAPENEM; HOMOSERINE; LACTONE; PIGMENT; PRODIGIOSIN;

ANTIBIOTIC BIOSYNTHESIS; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BIOASSAY; CONTROLLED STUDY; COSMID; GENE ISOLATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PECTOBACTERIUM CAROTOVORUM; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SERRATIA; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BASE SEQUENCE; CARBAPENEMS; CLONING, MOLECULAR; COSMIDS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PECTOBACTERIUM CAROTOVORUM; PLASMIDS; PRODIGIOSIN; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SERRATIA;

BACTERIA (MICROORGANISMS); ERWINIA; NEGIBACTERIA; PECTOBACTERIUM CAROTOVORUM; PROKARYOTA; SERRATIA; SERRATIA SP.; SERRATIA SP. ATCC 39006;

EID: 0034016854     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2000.01872.x     Document Type: Article

References (81)

1. Aucken, H.M., and Pitt, T.L. (1998) Antibiotic resistance and putative virulence factors of Serratia marcescens with respect to O and K serotypes. J Med Microbiol 47: 1105-1113.
2. Bainton, N.J., Stead, P., Chhabra, S.R., Bycroft, B.W., Salmond, G.P.C., Stewart, G.S.A.B., et al. (1992a) N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem J 288: 997-1004.
3. Bainton, N.J., Bycroft, B.W., Chhabra, S.R., Stead, P., Gledhill, L., Hill, P., et al. (1992b) A general role for the lux autoinducer in bacterial cell signalling: control of antibiotic biosynthesis in Erwinia. Gene 116: 87-91.
4. Blattner, F.R., Plunkett, G., Bloch, C.A., Perna, N.T., Burland, V., Riley, M., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1470.
5. Boger, D.L., and Patel, M. (1987) Total synthesis of prodigiosin. Tetrahedron Lett 48: 2499-2502.
6. Bu'Lock, J.D. (1961) Intermediary metabolism and antibiotic synthesis. Annu Rev Microbiol 3: 293-342.
7. Burger, S.R., and Bennet, J.W. (1985) Droplet enrichment factors of pigmented and nonpigmented Serratia marcescens: Possible selective function for prodigiosin. Appl Environ Microbiol 50: 487-490.
8. Bycroft, B.W., Maslen, C., Box, S.J., Brown, A., and Tyler, J.W. (1987) The isolation and characterisation of (3R,5R)-and (3S,5R)-carbapenem-3-carboxylic acid from Serratia and Erwinia species and their putative biosynthetic role. J Chem Soc Chem Commun 21: 1623-1625.
9. Bycroft, B.W., Maslen, C., Box, S.J., Brown, A., and Tyler, J.W. (1988) The biosynthetic implications of acetate and glutamate incorporation into (3R,5R)-carbapenam-3-carboxylic acid and (5R)-carbapen-2-em-3-carboxylic acid by Serratia sp. J Antibiot 41: 1231-1242.
10. Chang, A.C.Y., and Cohen, S.N. (1978) Construction and characterisation of a amplifiable multicopy DNA cloning vehicle derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
11. Cho, S.G., and Choi, Y.J. (1998) Characterization of the xaiF gene encoding a novel xylanase-activity-increasing factor, XaiF. J Microbiol Biotechnol 8: 378-387.
12. Coco, E.A., Narva, K.E., and Feitelson, J.S. (1991) New classes of Streptomyces coelicolor A3(2) mutants blocked in undecylprodigiosin (Red) biosynthesis. Mol Gen Genet 227: 28-32.
13. Cohen, S.P., Hachler, H., and Levy, S.B. (1993) Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli. J Bacteriol 175: 1484-1492.
14. Cox, A.R.J., Thomson, N.R., Bycroft, B., Stewart, G.S.A.B., Williams, P., and Salmond, G.P.C. (1998) A pheromone-independent CarR protein controls carbapenem antibiotic synthesis in the opportunistic human pathogen Serratia marcescens. Microbiology 144: 201-209.
15. D'Alessio, R., and Rossie, A. (1996) Short synthesis of undecylprodigiosine. A new route to 2′,2′-bipyrrolyl-pyrromethene systems. Syn Lett 6: 513-514.
16. D'Auria, M., DeLuca, E., Mauriello, G., and Racioppi, R. (1999) A short synthesis of a thienyl analogue of undecylprodigiosin. Syn Commun 29: 35-42.
17. Dauenhauer, S.A., Hull, R.A., and Williams, R.P. (1984) Cloning and expression in E. coli of Serratia marcescens genes encoding prodigiosin biosynthesis. J Bacteriol 158: 1128-1132.
18. De Lorenzo, V., Herrero, M., Jakubzik, U., and Timmis, K.N. (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172: 6568-6572.
19. De Vries, G.E., Raymond, C.K., and Ludwig, R.A. (1984) Extension of bacteriophage I host range: selection, cloning and characterisation of a constitutive I receptor gene. Proc Natl Acad Sci USA 81: 6080-6084.
20. Dehoux, P., and Cossart, P. (1995) Homologies between salmolysin and some bacterial regulatory proteins. Mol Microbiol 15: 591-592.
21. Demain, A. L. (1995) Why do microorganisms produce antimicrobials? In Fifty Years of Antimicrobials: Past Perspectives and Future Trends. Symposium 53. Hunter, P.A., Darby, G.K., and Russell, N.J. (eds). Cambridge: Society for General Microbiology, pp. 205-228.
22. Ding, M., and Williams, R.P. (1983) Biosynthesis of prodigiosin by white strains of Serratia marcescens isolated from patients. J Clin Microbiom: 476-480.
23. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D.R. (1980) Broad host range DNA cloning systems for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci USA 77: 7347-7351.
24. Eberl, L., Winson, M.K., Sternberg, C., Stewart, G.S.A.B., Christiansen, G., Chhabra, S.R., et al. (1996) Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol 20: 127-136.
25. Eberl, L., Molin, S., and Givskov, M. (1999) Surface motility of Serratia liquefaciens MG1. J Bacteriol 181: 1703-1712.
26. Feitelson, J.S., and Hopwood, D.A. (1983) Cloning of a Streptomyces gene for an O-methyltransferase involved in antibiotic biosynthesis. Mol Gen Genet 190: 394-398.
27. Fuqua, W.C., Winans, S.C., and Greenberg, E.P. (1994) Quorum sensing in bacteria - the LuxR-Luxl family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269-275.
28. Gerber, N.N. (1975) Prodigiosin-like pigments. CRC Crit Rev Microbiol 462: 469-485.
29. Givskov, M., Eberl, L., and Molin, S. (1997) Control of exoenzyme production, motility and cell differentiation in Serratia liquefaciens. FEMS Microbiol Lett 148: 115-122.
30. Goluszko, P., Nowicki, B., Goluszko, E., Nowicki, S., Kaul, A., and Pham, T. (1995) Association of colony variation in Serratia marcescens with the differential expression of protease and type 1 fimbriae. FEMS Microbiol Lett 133: 41-45.
31. Grimont, P.A.D., and Grimont, F. (1978) The genus Serratia. Annu Rev Microbiol 32: 221-248.
32. Grimont, P.A.D., and Grimont, F. (1984) Genus VIII. Serratia. In Bergy's Manual of Systematic Bacteriology, Vol. 1. Krieg, N.R., and Holt, J.G. (eds). Baltimore: The Williams and Wilkins Co., pp. 477-484.
33. Hacker, J., Blum-Oehler, G., Muhldorfer, I., and Tschape, H. (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23: 1089-1097.
34. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
35. Hines, D.A., Saurugger, P.M., Ihler, G.M., and Benedik, M.J. (1988) Genetic analysis of extracellular proteins of Serratia marcescens. J Bacteriol 170: 4141-4146.
36. Holden, M.T.G., McGowan, S.J., Bycroft, B.W., Stewart, G.S.A.B., Williams, P., and Salmond, G.P.C. (1998) Cryptic carbapenem antibiotic production genes are widespread in Erwinia carotovora: facile frans activation by the carR transcriptional regulator. Microbiology 144: 1495-1508.
37. Hood, D.W., Heidstra, R., Swoboda, U.K., and Hodgson, D.A. (1992) Molecular genetic analysis of proline and tryptophan biosynthesis in Streptomyces coelicolor A3(2): interactions between primary and secondary metabolism. Gene 115: 5-12.
38. Kataoka, T., Magae, J., Nariuchi, H., Yamasaki, M., and Nagai, K. (1992) Enhancement by concanavalin A of the suppressive effect of prodigiosin 25-C on proliferation of murine splenocytes. J Antibiot 45: 1303-1312.
39. Magae, J., Miller, M.W., Nagai, K., and Shearer, G.M. (1996) Effect of metacycloprodigiosin, an inhibitor of killer T cells, on murine skin and heart transplants. J Antibiot 49: 86-90.
40. Malpartida, F., Niemi, J., Navarrete, R., and Hopwood, D.A. (1990) Cloning and expression in a heterologous host of the complete set of genes for the biosynthesis of the Streptomyces coelicolor antibiotic undecylprodigiosin. Gene 93: 91-99.
41. McClean, K.H., Winson, M.K., Fish, L., Taylor, A., Chhabra, S.R., Camara, M., et al. (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acyl homoserine lactones. Microbiology 143: 3703-3711.
42. McGowan, S.J., Sebaihia, M., Jones, S., Yu, B., Bainton, N., Chan, P.F., et al. (1995) Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional regulator. Microbiology 141: 541-550.
43. McGowan, S.J., Sebaihia, M., Porter, L.E., Stewart, G.S.A.B., Williams, P., Bycroft, B.W., et al. (1996) Analysis of bacterial carbapenem antibiotic production genes reveals a novel β-lactam biosynthetic pathway. Mol Microbiol 22: 415-426.
44. McGowan, S.J., Sebaihia, M., O'Leary, S., Hardie, K.R., Williams, P., Stewart, G.S.A.B., et al. (1997) Analysis of the carbapenem gene cluster of Erwinia carotovora: definition of the antibiotic biosynthetic genes and evidence for a novel β-lactam resistance mechanism. Mol Microbiol 26: 545-556.
45. McGowan, S.J., Bycroft, B.W., and Salmond, G.P.C. (1998) Bacterial production of carbapenems and clavams: evolution of β-lactam antibiotic pathways. Trends Microbiol 6: 203-208.
46. Mellies, J., Jose, J., and Meyer, T.F. (1997) The Neisseria gonorrhoeae gene aniA encodes an inducible nitrite reductase. Mol Gen Genet 256: 525-532.
47. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
48. Morrison, D.A. (1969) Prodigiosin synthesis in mutants of Serratia marcescens. J Bacteriol 91: 1599-1604.
49. Nakamura, A., Nagai, N., Ando, K., and Tamura, G. (1986) Selective suppressive by prodigiosin of the mitogenic response of murine splenocytes. J Antibiot 39: 1155-1159.
50. Narva, K.E., and Feitelson, J.S. (1990) Nucleotide sequence and transcriptional analysis of the redD locus of Streptomyces coelicolor A3(2). J Bacteriol 172: 326-333.
51. Ochsner, U.A., and Vasil, M.L. (1996) Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: cycle selection of iron-regulated genes. Proc Natl Acad Sci USA 93: 4409-4414.
52. Ohtsubo, H., Nyman, K., Doroszkiewicz, W., and Ohtsubo, E. (1981) Multiple copies of iso-insertion sequences of IS1 in Shigella dysenteriae chromosome. Nature 292: 640-643.
53. Oscarsson, J., Mizunoe, Y., Uhlin, B.E., and Haydon, D.J. (1996) Induction of haemolytic activity in Escberichia coli by the slyA gene product. Mol Microbiol 20: 191-199.
54. Parker, W.L., Rathnum, M.L., Wells, J.S., Trejo, W.H., Principe, P.A., and Sykes, R.B. (1982) SQ 27,860, a simple carbapenem produced by species of Serratia and Erwinia. J Antibiot 35: 653-660.
55. Parsons, G.D., Donly, B.C., and Mackie, G.A. (1988) Mutations in the leader sequence and initiation codon of the gene for ribosome protein S20 (rpsT) affect both translational efficiency and autoregulation. J Bacteriol 170: 2495-2492.
56. Paruchuri, D.K., and Harshey, R.M. (1987) Flagella variation in Serratia marcescens is associated with colour variation. J Bacteriol 169: 61-65.
57. Pirhonen, M., Flego, D., Heikinhiemo, R., and Palva, E.T. (1993) A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J 12: 2467-2476.
58. Reverchon, R., Nasser, W., and Robert-Baudouy, J. (1994) pecS: a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi. Mol Microbiol 11: 1127-1139.
59. Ringquist, S., Shinedling, S., Barrick, D., Green, L., Binkley, J., Stormo, G.D., et al. (1992) Translation initiation in Escherichia coli: sequences within the ribosome-binding site. Mol Microbiol 6: 1219-1229.
60. Ryohei, F.T., Magae, M., Yamashita, K.N., and Makari, Y. (1992) Immunomodulating properties of prodigiosin 25-C. An antibiotic which preferentially suppresses induction of cytotoxic T-cells. J Antibiot 45: 1295-1302.
61. Salmond, G.P.C., Bycroft, B.W., Stewart, G.S.A.B., and Williams, P. (1995) The bacterial 'enigma': cracking the code of cell-cell communication. Mol Microbiol 16: 615-624.
62. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
63. Selvaraj, G., Fong, Y.C., and Iyer, V.N. (1984) A portable DNA sequence carrying the cohesive site (cos) of bacteriophage I and the mob (mobilisation) region of the broad-host-range plasmid RK2: a module for the construction of new cosmids. Gene 32: 235-241.
64. Shapiro, J.A. (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52: 81-104.
65. Shaw, P.D., Ping, G., Galy, S.L., Cha, C., Cronan, J.E. Jr, Rinehart, K.L., et al. (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci USA 94: 6036-6041.
66. Shea, C.M., and McIntosh, M.A. (1991) Nucleotide sequence and genetic organisation of the ferric enterobactin transport system: homology to other periplasmic binding protein-dependent systems in Escherichia coli. Mol Microbiol 5: 1415-1428.
67. Sole, M., Rius, N., Francia, A., and Loren, J.G. (1994) The effect of pH on prodigiosin production by non-proliferating cells of Serratia marcescens. Lett Appl Microbiol 19: 341-344.
68. Staudenmaier, H., Vanhove, B., Yaraghi, Z., and Braun, V. (1989) Nucleotide-sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-protein-dependent transport mechanism for iron (III) dicitrate in Escherichia coli. J Bacteriol 171: 2626-2633.
69. Swift, S., Winson, M.K., Chan, P.F., Bainton, N.J., Birdsall, M., Reeves, P.J., et al. (1993) A novel strategy for the isolation of luxl homologues: evidence for the widespread distribution of a luxR. luxl superfamily in enteric bacteria. Mol Microbiol 10: 511-520.
70. Tabor, S., and Richardson, C.C. (1985) A bacteriophage T7 RNA polymerase promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 82: 1074-1078.
71. Thomson, N.B., Cox, A., Bycroft, B.W., Stewart, G.S.A.B., Williams, P., and Salmond, G.P.C. (1997) The Rap and Hor proteins of Erwinia, Serratia and Yersinia: a novel subgroup in a growing superfamily of proteins regulating diverse physiological processes in bacterial pathogens. Mol Microbiol 26: 531-544.
72. Toth, I., Perombelom, M.C.M., and Salmond, G.P.C. (1993) Bacteriophage fKP mediated generalised transduction in Erwinia carotovora subsp. carotovora. J Gen Microbiol 139: 2705-2709.
73. Tsao, S., Rudd, B.A.M., He, X., Chang, C., and Floss, H.G. (1985) Identification of a red pigment from Streptomyces coelicolor A3(2) as a mixture of prodigiosin derivatives. J Antibiot 38: 128-131.
74. Tsuji, R.F., Yamamoto, M., Nakamura, A., Kataoka, T., Magae, J., Nagai, K., et al. (1990) Selective immunosuppression of prodigiosin 25-C and FK506 in the murine immune-system. J Antibiot 43: 1293-1301.
75. Tsuji, R.F., Magae, J., Yamashita, M., Nagai, K., and Yamasaki, M. (1992) Immunomodulating properties of prodigiosin 25-C, an antibiotic which preferentially suppresses induction of cytotoxic T-cells. J Antibiot 45: 1295-1302.
76. Vokes, S.A., Reeves, S.A., Torres, A.G., and Payne, S.M. (1999) The aerobactin iron transport system genes in Shigella flexneri are present within a pathogenicity island. Mol Microbiol 33: 63-73.
77. Wasserman, H.H., and Lombardo, L.J. (1989) The chemistry of vicinal tricarbonyls. A total synthesis of prodigiosin. Tetrahedron Lett 30: 1725-1728.
78. Welch, M., Todd, D.E., Whitehead, N.A., McGowan, S.J., Bycroft, B.W., and Salmond, G.P.C. (2000) N-acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia. EMBO J 19: 631-641.
79. Williams, R.P., and Quadri, S.M. (1980) The pigments of Serratia. In The Genus Serratia. Von Graevenitz, A., and Rubin, S.J. (eds). Boca Raton, FL: CRC Press Inc, pp. 31-75.
80. Williams, R.P., Gott, C.L., Quadri, S.M.H., and Scott, R.H. (1971) Influence of temperature of incubation and type of growth media on pigmentation in Serratia marcescens. J Bacteriol 106: 438-443.
81. Winson, M.K., Swift, S., Fish, L., Throup, J.P., Jorgensen, F., Chhabra, S.R., et al. (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163: 185-192.