Serratia marcescens quinoprotein glucose dehydrogenase activity mediates medium acidification and inhibition of prodigiosin production by glucose

Applied and Environmental Microbiology

Volumn 78, Issue 17, 2012, Pages 6225-6235

  Fender, James E ^a   Bender, Cody M ^a   Stella, Nicholas A ^a   Lahr, Roni M ^a   Kalivoda, Eric J ^a,b   Shanks, Robert M Q ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE PIGMENTS; BIOSYNTHETIC GENE; CYCLIC AMP (CAMP); D-GLUCONATES; D-GLUCONIC ACIDS; D-GLUCOSE; DATA SUPPORT; GENETIC LOCUS; GENETIC PATHWAYS; INHIBITORY EFFECT; LARGE-SCALE PRODUCTION; MODEL ORGANISMS; PH-DEPENDENT; PRODIGIOSIN; PYRROLOQUINOLINE QUINONE; QUINOPROTEIN GLUCOSE DEHYDROGENASE; QUINOPROTEINS; SECONDARY METABOLITES; SERRATIA MARCESCENS; TRANSCRIPTIONAL CONTROL; TRANSPOSON MUTAGENESIS; UBIQUINONE;

BIOSYNTHESIS; GENES; METABOLITES; PH EFFECTS;

GLUCOSE;

GLUCOSE; GLUCOSE DEHYDROGENASE; GLUCOSE DEHYDROGENASE (PYRROLOQUINOLINE QUINONE); GLUCOSE DEHYDROGENASE (PYRROLOQUINOLINE-QUINONE); PRODIGIOSIN;

ACIDIFICATION; BACTERIUM; ENZYME ACTIVITY; GLUCOSE; INHIBITION; INHIBITOR; SECONDARY METABOLITE;

ARTICLE; BIOLOGICAL MODEL; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PH; SERRATIA MARCESCENS; TRANSPOSON;

BIOSYNTHETIC PATHWAYS; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; GLUCOSE DEHYDROGENASES; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; MUTAGENESIS, INSERTIONAL; PRODIGIOSIN; SERRATIA MARCESCENS;

SERRATIA MARCESCENS;

EID: 84866160387     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01778-12     Document Type: Article

References (60)

1. Anthony C. 2004. The quinoprotein dehydrogenases for methanol and glucose. Arch. Biochem. Biophys. 428:2-9.
2. Ben Farhat M, et al. 2009. Characterization of the mineral phosphate solubilizing activity of Serratia marcescens CTM 50650 isolated from the phosphate mine of Gafsa. Arch. Microbiol. 191:815-824.
3. Bouvet OM, Grimont PA. 1988. Extracellular oxidation of D-glucose by some members of the Enterobacteriaceae. Ann. Inst. Pasteur Microbiol. 139:59-77.
4. Bunting MI, Robinow CF, Bunting H. 1949. Factors affecting the elaboration of pigment and polysaccharide by Serratia marcescens. J. Bacteriol. 58:114.
5. Burger SR, Bennett JW. 1985. Droplet enrichment factors of pigmented and nonpigmented Serratia marcescens: possible selective function for prodigiosin. Appl. Environ. Microbiol. 50:487-490.
6. Chang SC, Wei YH, Wei DL, Chen YY, Jong SC. 1991. Factors affecting the production of eremofortin C and PR toxin in Penicillium roqueforti. Appl. Environ. Microbiol. 57:2581-2585.
7. Chiang SL, Rubin EJ. 2002. Construction of a mariner-based transposon for epitope-tagging and genomic targeting. Gene 296:179-185.
8. Clements-Jewery S. 1976. The reversal of glucose repressed prodigiosin production in Serratia marcescens by the cyclic 3'5'-adenosine monophosphate inhibitor theophylline. Experientia 32:421-422.
9. Cleton-Jansen AM, Goosen N, Fayet O, van de Putte P. 1990. Cloning, mapping, and sequencing of the gene encoding Escherichia coli quinoprotein glucose dehydrogenase. J. Bacteriol. 172:6308-6315.
10. Dauenhauer SA, Hull RA, Williams RP. 1984. Cloning and expression in Escherichia coli of Serratia marcescens genes encoding prodigiosin biosynthesis. J. Bacteriol. 158:1128-1132.
11. Espeso EA, Tilburn J, Arst HN, Jr, Penalva MA. 1993. pH regulation is a major determinant in expression of a fungal penicillin biosynthetic gene. EMBO J. 12:3947-3956.
12. Fineran PC, Everson L, Slater H, Salmond GP. 2005. A GntR family transcriptional regulator (PigT) controls gluconate-mediated repression and defines a new, independent pathway for regulation of the tripyrrole antibiotic, prodigiosin, in Serratia. Microbiology 151:3833-3845.
13. Fineran PC, Williamson NR, Lilley KS, Salmond GP. 2007. Virulence and prodigiosin antibiotic biosynthesis in Serratia are regulated pleiotropically by the GGDEF/EAL domain protein, PigX. J. Bacteriol. 189:7653-7662.
14. Gerber NN. 1975. Prodigiosin-like pigments. Crit. Rev. Microbiol. 3:469-485.
15. Giri AV, Anandkumar N, Muthukumaran G, Pennathur G. 2004. A novel medium for the enhanced cell growth and production of prodigiosin from Serratia marcescens isolated from soil. BMC Microbiol. 4:11.
16. Grimont PA, Grimont F. 1978. Biotyping of Serratia marcescens and its use in epidemiological studies. J. Clin. Microbiol. 8:73-83.
17. Gristwood T, Fineran PC, Everson L, Salmond GP. 2008. PigZ, a TetR/AcrR family repressor, modulates secondary metabolism via the expression of a putative four-component resistance-nodulation-cell-division efflux pump, ZrpADBC, in Serratia sp. ATCC 39006. Mol. Microbiol. 69:418-435.
18. Gristwood T, Fineran PC, Everson L, Williamson NR, Salmond GP. 2009. The PhoBR two-component system regulates antibiotic biosynthesis in Serratia in response to phosphate. BMC Microbiol. 9:112.
19. Gristwood T, McNeil MB, Clulow JS, Salmond GP, Fineran PC. 2011. PigS and PigP regulate prodigiosin biosynthesis in Serratia via differential control of divergent operons, which include predicted transporters of sulfur-containing molecules. J. Bacteriol. 193:1076-1085.
20. Haavik HI. 1974. Studies on the formation of bacitracin by Bacillus licheniformis: role of catabolite repression and organic acids. J. Gen. Microbiol. 84:321-326.
21. Haddix PL, et al. 2008. Kinetic analysis of growth rate, ATP, and pigmentation suggests an energy-spilling function for the pigment prodigiosin of Serratia marcescens. J. Bacteriol. 190:7453-7463.
22. Hameeda B, Reddy YH, Rupela OP, Kumar GN, Reddy G. 2006. Effect of carbon substrates on rock phosphate solubilization by bacteria from composts and macrofauna. Curr. Microbiol. 53:298-302.
23. Harris AK, et al. 2004. The Serratia gene cluster encoding biosynthesis of the red antibiotic, prodigiosin, shows species- and strain-dependent genome context variation. Microbiology 150:3547-3560.
24. Heinemann B, Howard AJ, Palocz HJ. 1970. Influence of dissolved oxygen levels on production of L-asparaginase and prodigiosin by Serratia marcescens. Appl. Microbiol. 19:800-804.
25. Hucho F, Wallenfels K. 1972. Glucono-lactonase from Escherichia coli. Biochim. Biophys. Acta 276:176-179.
26. James PD, Edwards C, Dawson M. 1991. The effects of temperature, pH and growth rate on secondary metabolism in Streptomyces thermoviolaceus grown in a chemostat. J. Gen. Microbiol. 137:1715-1720.
27. Kalivoda EJ, et al. 2010. Cyclic AMP negatively regulates prodigiosin production by Serratia marcescens. Res. Microbiol. 161:158-167.
28. Kalivoda EJ, Stella NA, O'Dee DM, Nau GJ, Shanks RM. 2008. The cyclic AMP-dependent catabolite repression system of Serratia marcescens mediates biofilm formation through regulation of type 1 fimbriae. Appl. Environ. Microbiol. 74:3461-3470.
29. Krajewski V, et al. 2010. Metabolic engineering of Gluconobacter oxydans for improved growth rate and growth yield on glucose by elimination of gluconate formation. Appl. Environ. Microbiol. 76:4369-4376.
30. Krishnaraj PU, Goldstein AH. 2001. Cloning of a Serratia marcescens DNA fragment that induces quinoprotein glucose dehydrogenasemediated gluconic acid production in Escherichia coli in the presence of stationary phase Serratia marcescens. FEMS Microbiol. Lett. 205:215-220.
31. Kulasekara HD, et al. 2005. A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol. Microbiol. 55:368-380.
32. Matsushita K, Nonobe M, Shinagawa E, Adachi O, Ameyama M. 1987. Reconstitution of pyrroloquinoline quinone-dependent D-glucose oxidase respiratory chain of Escherichia coli with cytochrome o oxidase. J. Bacteriol. 169:205-209.
33. Matsushita K, Shinagawa E, Adachi O, Ameyama M. 1989. Quinoprotein D-glucose dehydrogenase of the Acinetobacter calcoaceticus respiratory chain: membrane-bound and soluble forms are different molecular species. Biochemistry 28:6276-6280.
34. Miller VL, Mekalanos JJ. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575.
35. Mustafa G, et al. 2008. Menaquinone as well as ubiquinone as a bound quinone crucial for catalytic activity and intramolecular electron transfer in Escherichia coli membrane-bound glucose dehydrogenase. J. Biol. Chem. 283:28169-28175.
36. Ordentlich A, Elad Y, Chet I. 1987. Rhizosphere colonization by Serratia marcescens for the control of Sclerotium rolfsii. Soil Biol. Biochem. 19:747-751.
37. O'Toole GA, et al. 1999. Genetic approaches to the study of biofilms. Methods Enzymol. 310:91-109.
38. Perez-Tomas R, Vinas M. 2010. New insights on the antitumoral properties of prodiginines. Curr. Med. Chem. 17:2222-2231.
39. Pocker Y, Green E. 1973. Hydrolysis of D-glucono-delta-lactone. I. General acid-base catalysis, solvent deuterium isotope effects, and transition state characterization. J. Am. Chem. Soc. 95:113-119.
40. Poon WW, et al. 2000. Identification of Escherichia coli ubiB, a gene required for the first monooxygenase step in ubiquinone biosynthesis. J. Bacteriol. 182:5139-5146.
41. Rius N, Sole M, Fancia A, Loren JG. 1994. Buffering capacity of pigmented and nonpigmented strains of Serratia marcescens. Appl. Environ. Microbiol. 60:2152-2154.
42. Rosenberg M. 1984. Isolation of pigmented and nonpigmented mutants of Serratia marcescens with reduced cell surface hydrophobicity. J. Bacteriol. 160:480-482.
43. Rosenberg M, et al. 1986. Cell surface hydrophobicity of pigmented and nonpigmented clinical Serratia marcescens strains. Infect. Immun. 51:932-935.
44. Sato T, et al. 1998. Prodigiosins as a new group of H+/Cl- symporters that uncouple proton translocators. J. Biol. Chem. 273:21455-21462.
45. Shah AJ, Tilburn J, Adlard MW, Arst HN, Jr. 1991. pH regulation of penicillin production in Aspergillus nidulans. FEMS Microbiol. Lett. 61:209-212.
46. Shanks RM, Caiazza NC, Hinsa SM, Toutain CM, O'Toole GA. 2006. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl. Environ. Microbiol. 72:5027-5036.
47. Shanks RM, Kadouri DE, MacEachran DP, O'Toole AG. 2009. New yeast recombineering tools for bacteria. Plasmid 62:88-97.
48. Shanks RM, et al. 2007. A Serratia marcescens OxyR homolog mediates surface attachment and biofilm formation. J. Bacteriol. 189:7262-7272.
49. Silverman MP, Munoz EF. 1973. Effect of iron and salt on prodigiosin synthesis in Serratia marcescens. J. Bacteriol. 114:999-1006.
50. Sole M, Francia A, Rius N, Loren JG. 1997. The role of pH in the "glucose effect" on prodigiosin production by non-proliferating cells of Serratia marcescens. Lett. Appl. Microbiol. 25:81-84.
51. Sole M, Rius N, Francia A, Loren JG. 1994. The effect of pH on prodigiosin production by non-proliferating cells of Serratia marcescens. Lett. Appl. Microbiol. 19:341-344.
52. Sole M, Rius N, Loren JG. 2000. Rapid extracellular acidification induced by glucose metabolism in non-proliferating cells of Serratia marcescens. Int. Microbiol. 3:39-43.
53. Stella NA, Kalivoda EJ, O'Dee DM, Nau GJ, Shanks RM. 2008. Catabolite repression control of flagellum production by Serratia marcescens. Res. Microbiol. 159:562-568.
54. Tanikawa T, Nakagawa Y, Matsuyama T. 2006. Transcriptional downregulator HexS controlling prodigiosin and serrawettin W1 biosynthesis in Serratia marcescens. Microbiol. Immunol. 50:587-596.
55. Tarighi S, et al. 2008. The PA4204 gene encodes a periplasmic gluconolactonase (PpgL) which is important for fitness of Pseudomonas aeruginosa. Microbiology 154:2979-2990.
56. Williams RP, Goldschmidt ME, Gott CL. 1965. Inhibition by temperature of the terminal step in biosynthesis of prodigiosin. Biochem. Biophys. Res. Commun. 19:177-181.
57. Williams RP, Gott CL, Qadri SM, Scott RH. 1971. Influence of temperature of incubation and type of growth medium on pigmentation in Serratia marcescens. J. Bacteriol. 106:428-443.
58. Williamson NR, Fineran PC, Leeper FJ, Salmond GP. 2006. The biosynthesis and regulation of bacterial prodiginines. Nat. Rev. Microbiol. 4:887-899.
59. Williamson NR, Fineran PC, Ogawa W, Woodley LR, Salmond GP. 2008. Integrated regulation involving quorum sensing, a two-component system, a GGDEF/EAL domain protein and a posttranscriptional regulator controls swarming and RhlA-dependent surfactant biosynthesis in Serratia. Environ. Microbiol. 10:1202-1217.
60. Witney FR, Failla ML, Weinberg ED. 1977. Phosphate inhibition of secondary metabolism in Serratia marcescens. Appl. Environ. Microbiol. 33:1042-1046.