A Serratia marcescens PigP Homolog Controls Prodigiosin Biosynthesis, Swarming Motility and Hemolysis and Is Regulated by cAMP-CRP and HexS

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Shanks, Robert M Q ^a   Lahr, Roni M ^a   Stella, Nicholas A ^a   Arena, Kristin E ^a   Brothers, Kimberly M ^a   Kwak, Daniel H ^a   Liu, Xinyu ^a   Kalivoda, Eric J ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; C REACTIVE PROTEIN; CYCLIC AMP; PIGP PROTEIN; PRODIGIOSIN; SERRATAMOLIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HEXS; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE AMPLIFICATION; GENE CONTROL; GENE MUTATION; HEMOLYSIS; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PHENOTYPE; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SERRATIA MARCESCENS; SWARMING MOTILITY; TRANSCRIPTION INITIATION;

BACTERIAL PROTEINS; DEPSIPEPTIDES; ERYTHROCYTES; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC COMPLEMENTATION TEST; HEMOLYSIS; HEXOSYLTRANSFERASES; HUMANS; MEMBRANE PROTEINS; MOVEMENT; MUTATION; OPERON; PRODIGIOSIN; SEQUENCE HOMOLOGY, AMINO ACID; SERRATIA MARCESCENS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84874571086     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057634     Document Type: Article

References (73)

1. Mahlen SD, (2011) Serratia infections: from military experiments to current practice. Clin Microbiol Rev 24: 755-791.
2. Diekema DJ, Pfaller MA, Jones RN, Doern GV, Winokur PL, et al. (1999) Survey of bloodstream infections due to gram-negative bacilli: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, and Latin America for the SENTRY Antimicrobial Surveillance Program, 1997. Clin Infect Dis 29: 595-607.
3. Richards MJ, Edwards JR, Culver DH, Gaynes RP, (2000) Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol 21: 510-515.
4. Jones RN, (2010) Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clin Infect Dis 51Suppl 1: S81-87.
5. Verhamme KM, De Coster W, De Roo L, De Beenhouwer H, Nollet G, et al. (2007) Pathogens in early-onset and late-onset intensive care unit-acquired pneumonia. Infect Control Hosp Epidemiol 28: 389-397.
6. Laupland KB, Parkins MD, Gregson DB, Church DL, Ross T, et al. (2008) Population-based laboratory surveillance for Serratia species isolated in a large Canadian health region. Eur J Clin Microbiol Infect Dis 27: 89-95.
7. Hume EB, Conerly LL, Moreau JM, Cannon BM, Engel LS, et al. (1999) Serratia marcescens keratitis: strain-specific corneal pathogenesis in rabbits. Curr Eye Res 19: 525-532.
8. Hume EB, Willcox MD, (2004) Emergence of Serratia marcescens as an ocular surface pathogen. Arch Soc Esp Oftalmol 79: 475-477.
9. Butler MT, Wang Q, Harshey RM, (2010) Cell density and mobility protect swarming bacteria against antibiotics. Proc Natl Acad Sci U S A 107: 3776-3781.
10. Kearns DB, (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8: 634-644.
11. Overhage J, Bains M, Brazas MD, Hancock RE, (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190: 2671-2679.
12. Allison C, Lai HC, Hughes C, (1992) Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol Microbiol 6: 1583-1591.
13. Fraser GM, Claret L, Furness R, Gupta S, Hughes C, (2002) Swarming-coupled expression of the Proteus mirabilis hpmBA haemolysin operon. Microbiology 148: 2191-2201.
14. Walker KE, Moghaddame-Jafari S, Lockatell CV, Johnson D, Belas R, (1999) ZapA, the IgA-degrading metalloprotease of Proteus mirabilis, is a virulence factor expressed specifically in swarmer cells. Mol Microbiol 32: 825-836.
15. Wang WB, Chen IC, Jiang SS, Chen HR, Hsu CY, et al. (2008) Role of RppA in the regulation of polymyxin b susceptibility, swarming, and virulence factor expression in Proteus mirabilis. Infect Immun 76: 2051-2062.
16. Matsuyama T, Sogawa M, Nakagawa Y, (1989) Fractal spreading growth of Serratia marcescens which produces surface active exolipids. FEMS Microbiol Lett 52: 243-246.
17. O'Rear J, Alberti L, Harshey RM, (1992) Mutations that impair swarming motility in Serratia marcescens 274 include but are not limited to those affecting chemotaxis or flagellar function. J Bacteriol 174: 6125-6137.
18. Matsuyama T, Bhasin A, Harshey RM, (1995) Mutational analysis of flagellum-independent surface spreading of Serratia marcescens 274 on a low-agar medium. J Bact 177: 987-991.
19. Sunaga S, Li H, Sato Y, Nakagawa Y, Matsuyama T, (2004) Identification and characterization of the pswP gene required for the parallel production of prodigiosin and serrawettin W1 in Serratia marcescens. Microbiol Immunol 48: 723-728.
20. Li H, Tanikawa T, Sato Y, Nakagawa Y, Matsuyama T, (2005) Serratia marcescens gene required for surfactant serrawettin W1 production encodes putative aminolipid synthetase belonging to nonribosomal peptide synthetase family. Microbiol Immunol 49: 303-310.
21. Tanikawa T, Nakagawa Y, Matsuyama T, (2006) Transcriptional downregulator HexS controlling prodigiosin and serrawettin W1 biosynthesis in Serratia marcescens. Microbiol Immunol 50: 587-596.
22. Shanks RM, Stella NA, Lahr RM, Wang S, Veverka TI, et al. (2012) Serratamolide is a hemolytic factor produced by Serratia marcescens. PLoS One 7: e36398.
23. Allison C, Coleman N, Jones PL, Hughes C, (1992) Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect Immun 60: 4740-4746.
24. Carpinella MC, De Bellis L, Joray MB, Sosa V, Zunino PM, et al. (2011) Inhibition of development, swarming differentiation and virulence factors in Proteus mirabilis by an extract of Lithrea molleoides and its active principle (Z,Z)-5-(trideca-4′,7′-dienyl)-resorcinol. Phytomedicine 18: 994-997.
25. Dacheux D, Goure J, Chabert J, Usson Y, Attree I, (2001) Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol Microbiol 40: 76-85.
26. Givaudan A, Lanois A, (2000) flhDC, the flagellar master operon of Xenorhabdus nematophilus: requirement for motility, lipolysis, extracellular hemolysis, and full virulence in insects. J Bacteriol 182: 107-115.
27. Hsueh YH, Somers EB, Lereclus D, Ghelardi E, Wong AC, (2007) Biosurfactant production and surface translocation are regulated by PlcR in Bacillus cereus ATCC 14579 under low-nutrient conditions. Appl Environ Microbiol 73: 7225-7231.
28. Lin CS, Horng JT, Yang CH, Tsai YH, Su LH, et al. (2010) RssAB-FlhDC-ShlBA as a major pathogenesis pathway in Serratia marcescens. Infect Immun 78: 4870-4881.
29. Ulrich RL, Hines HB, Parthasarathy N, Jeddeloh JA, (2004) Mutational analysis and biochemical characterization of the Burkholderia thailandensis DW503 quorum-sensing network. J Bacteriol 186: 4350-4360.
30. Bhakdi S, Tranum-Jensen J, (1991) Alpha-toxin of Staphylococcus aureus. Microbiol Rev 55: 733-751.
31. Braun V, Focareta T, (1991) Pore-forming bacterial protein hemolysins (cytolysins). Crit Rev Microbiol 18: 115-158.
32. Schnupf P, Portnoy DA, (2007) Listeriolysin O: a phagosome-specific lysin. Microbes Infect 9: 1176-1187.
33. Dwivedi D, Jansen R, Molinari G, Nimtz M, Johri BN, et al. (2008) Antimycobacterial serratamolides and diacyl peptoglucosamine derivatives from Serratia sp. J Nat Prod 71: 637-641.
34. Wasserman HH, Keggi JJ, Mckeon JE, (1961) Serratamolide, a metabolic product of Serratia. J Am chem Soc 83: 4107-4108.
35. Kalivoda EJ, Stella NA, Aston MA, Fender JE, Thompson PP, et al. (2010) Cyclic AMP negatively regulates prodigiosin production by Serratia marcescens. Res Microbiol 161: 158-167.
36. Horng YT, Chang KC, Liu YN, Lai HC, Soo PC, (2010) The RssB/RssA two-component system regulates biosynthesis of the tripyrrole antibiotic, prodigiosin, in Serratia marcescens. Int J Med Microbiol 300: 304-312.
37. Horng YT, Deng SC, Daykin M, Soo PC, Wei JR, et al. (2002) The LuxR family protein SpnR functions as a negative regulator of N-acylhomoserine lactone-dependent quorum sensing in Serratia marcescens. Mol Microbiol 45: 1655-1671.
38. 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.
39. 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.
40. 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.
41. McNeil MB, Clulow JS, Wilf NM, Salmond GP, Fineran PC, (2012) SdhE is a conserved protein required for flavinylation of succinate dehydrogenase in bacteria. J Biol Chem 287: 18418-18428.
42. Ramsay JP, Salmond GP, (2012) Quorum sensing-controlled buoyancy through gas vesicles: Intracellular bacterial microcompartments for environmental adaptation. Commun Integr Biol 5: 96-98.
43. Wilf NM, Salmond GP, (2012) The stationary phase sigma factor, RpoS, regulates the production of a carbapenem antibiotic, a bioactive prodigiosin and virulence in the enterobacterial pathogen Serratia sp. ATCC 39006. Microbiology 158: 648-658.
44. Wilf NM, Williamson NR, Ramsay JP, Poulter S, Bandyra KJ, et al. (2011) The RNA chaperone, Hfq, controls two luxR-type regulators and plays a key role in pathogenesis and production of antibiotics in Serratia sp. ATCC 39006. Environ Microbiol 13: 2649-2666.
45. Williamson NR, Fineran PC, Leeper FJ, Salmond GP, (2006) The biosynthesis and regulation of bacterial prodiginines. Nat Rev Microbiol 4: 887-899.
46. Fineran PC, Slater H, Everson L, Hughes K, Salmond GP, (2005) Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol Microbiol 56: 1495-1517.
47. 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.
48. 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.
49. Gerber NN, (1975) Prodigiosin-like pigments. Crit Rev Microbiol 3: 469-485.
50. Vining LC (1990) Functions of secondary metabolites. Annu Rev Microbiol 44.
51. 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 post-transcriptional regulator controls swarming and RhlA-dependent surfactant biosynthesis in Serratia. Environ Microbiol 10: 1202-1217.
52. Rosenberg M, Blumberger Y, Judes H, Bar-Ness R, Rubinstein E, et al. (1986) Cell surface hydrophobicity of pigmented and nonpigmented clinical Serratia marcescens strains. Infect Immun 51: 932-935.
53. Rosenberg M, Kjelleberg S, (1986) Hydrophobic interactions: role in bacterial adhesion. Adv Microbial Ecol 9: 353-393.
54. 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.
55. Haddix PL, Jones S, Patel P, Burnham S, Knights K, 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.
56. 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.
57. Shanks RM, Stella NA, Kalivoda EJ, Doe MR, O'Dee DM, et al. (2007) A Serratia marcescens OxyR homolog mediates surface attachment and biofilm formation. J Bacteriol 189: 7262-7272.
58. Shanks RM, Donegan NP, Graber ML, Buckingham SE, Zegans ME, et al. (2005) Heparin stimulates Staphylococcus aureus biofilm formation. Infect Immun 73: 4596-4606.
59. Kowalski RP, Romanowski EG, Mah FS, Shanks RM, Gordon YJ, (2010) Topical levofloxacin 1.5% overcomes in vitro resistance in rabbit keratitis models. Acta Ophthalmol 88: e120-125.
60. Slater H, Crow M, Everson L, Salmond GP, (2003) Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and-independent pathways. Mol Microbiol 47: 303-320.
61. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
62. Marone M, Mozzetti S, De Ritis D, Pierelli L, Scambia G, (2001) Semiquantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample. Biol Proced Online 3: 19-25.
63. Stella NA, Fender JE, Lahr RM, Kalivoda EJ, Shanks RM (2012) The LysR transcription factor, HexS, is required for glucose inhibition of prodigiosin production by Serratia marcescens. Advances in Microbiology in press.
64. Morowitz MJ, Denef VJ, Costello EK, Thomas BC, Poroyko V, et al. (2011) Strain-resolved community genomic analysis of gut microbial colonization in a premature infant. Proc Natl Acad Sci U S A 108: 1128-1133.
65. Liaw SJ, Lai HC, Ho SW, Luh KT, Wang WB, (2003) Role of RsmA in the regulation of swarming motility and virulence factor expression in Proteus mirabilis. J Med Microbiol 52: 19-28.
66. Reimmann C, Ginet N, Michel L, Keel C, Michaux P, et al. (2002) Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148: 923-932.
67. Lai HC, Soo PC, Wei JR, Yi WC, Liaw SJ, et al. (2005) The RssAB two-component signal transduction system in Serratia marcescens regulates swarming motility and cell envelope architecture in response to exogenous saturated fatty acids. J Bacteriol 187: 3407-3414.
68. Shanks RMQ, Stella NA, Fender JE (2012) Mutation of crp mediates Serratia marcescens serralysin and global secreted protein production. Res Microbiol in press.
69. Fender JE, Bender CM, Stella NA, Lahr RM, Kalivoda EJ, et al. (2012) Serratia marcescens quinoprotein glucose dehydrogenase activity mediates medium acidification and inhibition of prodigiosin production by glucose. Appl Environ Microbiol 78: 6225-6235.
70. Matsuyama T, Murakami T, Fujita M, Fujita S, Yano I, (1986) Extracellular vesicle formation and biosurfactant production by Serratia marcescens. Journal of General Microbiology 132: 865-875.
71. 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.
72. 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.
73. Shanks RM, Kadouri DE, MacEachran DP, O'Toole G A, (2009) New yeast recombineering tools for bacteria. Plasmid 62: 88-97.