Genome analysis of Pseudoalteromonas flavipulchra JG1 reveals various survival advantages in marine environment

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Yu, Min ^a   Tang, Kaihao ^a   Liu, Jiwen ^a   Shi, Xiaochong ^a   Gulder, Tobias A M ^b   Zhang, Xiao Hua ^a  

^a OCEAN UNIVERSITY OF CHINA   (China)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Antibacterial metabolites; Genome analysis; Pseudoalteromonas flavipulchra; Quorum quenching; Survival advantages

Indexed keywords

ALGINIC ACID; BACTERIAL PROTEIN; CEPHALOSPORIN; CEPHALOSPORIN C; CHITINASE; CHLORAMPHENICOL; HYDROXYBENZOIC ACID; KANAMYCIN; N ACYLHOMOSERINE LACTONE; PENICILLIN DERIVATIVE; PHOSPHORUS; PROTEIN PFAP; RNA 16S; TETRACYCLINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; GAMMA BUTYROLACTONE DERIVATIVE;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIFUNGAL ACTIVITY; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBOHYDRATE SYNTHESIS; CELL DIVISION; CONTROLLED STUDY; DNA BASE COMPOSITION; DNA DAMAGE; GENE CLUSTER; GENE FUNCTION; GENE IDENTIFICATION; GENOME ANALYSIS; MARINE ENVIRONMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATIVE STRESS; PSEUDOALTEROMONAS; PSEUDOALTEROMONAS FLAVIPULCHRA JG1; QUORUM SENSING; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; GENETICS; METABOLISM; MULTIGENE FAMILY; PHYLOGENY;

BACTERIA (MICROORGANISMS); PSEUDOALTEROMONAS; PSEUDOALTEROMONAS FLAVIPULCHRA;

ACYL-BUTYROLACTONES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CHITINASE; DRUG RESISTANCE, BACTERIAL; GENOME, BACTERIAL; MULTIGENE FAMILY; PHYLOGENY; PSEUDOALTEROMONAS; QUORUM SENSING; SEQUENCE ANALYSIS, DNA;

EID: 84885458650     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-707     Document Type: Article

References (80)

1. Gauthier G, Gauthier M, Christen R. Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (emended) and Pseudoalteromonas gen. nov., and proposal of twelve new species combinations. Int J Syst Bacteriol 1995, 45:755-761. 10.1099/00207713-45-4-755, 7547295.
2. Hoyoux A, Jennes I, Dubois P, Genicot S, Dubail F, Francois JM, Baise E, Feller G, Gerday C. Cold-adapted beta-galactosidase from the Antarctic psychrophile Pseudoalteromonas haloplanktis. Appl Environ Microbiol 2001, 67:1529-1535. 10.1128/AEM.67.4.1529-1535.2001, 92765, 11282601.
3. Kobayashi T, Imada C, Hiraishi A, Tsujibo H, Miyamoto K, Inamori Y, Hamada N, Watanabe E. Pseudoalteromonas sagamiensis sp. nov., a marine bacterium that produces protease inhibitors. Int J Syst Evol Microbiol 2003, 53:1807-1811. 10.1099/ijs.0.02516-0, 14657108.
4. Egan S, Holmstrom C, Kjelleberg S. Pseudoalteromonas ulvae sp. nov., a bacterium with antifouling activities isolated from the surface of a marine alga. Int J Syst Evol Microbiol 2001, 51:1499-1504.
5. Bowman JP. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar Drugs 2007, 5:220-241. 10.3390/md504220, 2365693, 18463726.
6. James SG, Holmstrom C, Kjelleberg S. Purification and characterization of a novel antibacterial protein from the marine bacterium D2. Appl Environ Microbiol 1996, 62:2783-2788. 168063, 8702270.
7. Franks A, Haywood P, Holmstrom C, Egan S, Kjelleberg S, Kumar N. Isolation and structure elucidation of a novel yellow pigment from the marine bacterium Pseudoalteromonas tunicata. Molecules 2005, 10:1286-1291. 10.3390/10101286, 18007521.
8. Thomas T, Evans FF, Schleheck D, Mai-Prochnow A, Burke C, Penesyan A, Dalisay DS, Stelzer-Braid S, Saunders N, Johnson J, et al. Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment. PLoS One 2008, 3:e3252. 10.1371/journal.pone.0003252, 2536512, 18813346.
9. Jin G, Wang S, Yu M, Yan S, Zhang X-H. Identification of a marine antagonistic strain JG1 and establishment of a polymerase chain reaction detection technique based on the gyrB gene. Aquac Res 2010, 41:1867-1874.
10. Yu M, Wang J, Tang K, Shi X, Wang S, Zhu W-M, Zhang X-H. Purification and characterization of antibacterial compounds of Pseudoalteromonas flavipulchra JG1. Microbiology 2012, 158:835-842. 10.1099/mic.0.055970-0, 22194352.
11. Yu M, Tang K, Shi X, Zhang X-H. Genome sequence of Pseudoalteromonas flavipulchra JG1, a marine antagonistic bacterium with abundant antimicrobial metabolites. J Bacteriol 2012, 194:3735. 10.1128/JB.00598-12, 3393484, 22740664.
12. Egan S, James S, Kjelleberg S. Identification and characterization of a putative transcriptional regulator controlling the expression of fouling inhibitors in Pseudoalteromonas tunicata. Appl Environ Microbiol 2002, 68:372-378. 10.1128/AEM.68.1.372-378.2002, 126587, 11772647.
13. Medigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN, Cheung F, Cruveiller S, D'Amico S, Duilio A, et al. Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome research 2005, 15:1325-1335. 10.1101/gr.4126905, 1240074, 16169927.
14. Lucas-Elio P, Gomez D, Solano F, Sanchez-Amat A. The antimicrobial activity of marinocine, synthesized by Marinomonas mediterranea, is due to hydrogen peroxide generated by its lysine oxidase activity. J Bacteriol 2006, 188:2493-2501. 10.1128/JB.188.7.2493-2501.2006, 1428416, 16547036.
15. Faust A, Niefind K, Hummel W, Schomburg D. The structure of a bacterial L-amino acid oxidase from Rhodococcus opacus gives new evidence for the hydride mechanism for dehydrogenation. J Mol Biol 2007, 367:234-248. 10.1016/j.jmb.2006.11.071, 17234209.
16. Zaldivar J, Ingram LO. Effect of organic acids on the growth and fermentation of ethanologenic Escherichia coli LY01. Biotechnol Bioeng 1999, 66:203-210. 10.1002/(SICI)1097-0290(1999)66:4<203::AID-BIT1>3.0.CO;2-#, 10578090.
17. Nichols BP, Green JM. Cloning and sequencing of Escherichia coli ubiC and purification of chorismate lyase. J Bacteriol 1992, 174:5309-5316. 206367, 1644758.
18. Soballe B, Poole RK. Ubiquinone limits oxidative stress in Escherichia coli. Microbiology 2000, 146(Pt 4):787-796.
19. Watts KT, Mijts BN, Lee PC, Manning AJ, Schmidt-Dannert C. Discovery of a substrate selectivity switch in tyrosine ammonia-lyase, a member of the aromatic amino acid lyase family. Chem Biol 2006, 13:1317-1326. 10.1016/j.chembiol.2006.10.008, 17185227.
20. Xiang L, Moore BS. Inactivation, complementation, and heterologous expression of encP, a novel bacterial phenylalanine ammonia-lyase gene. J Biol Chem 2002, 277:32505-32509. 10.1074/jbc.M204171200, 12082112.
21. Xiang L, Moore BS. Biochemical characterization of a prokaryotic phenylalanine ammonia lyase. J Bacteriol 2005, 187:4286-4289. 10.1128/JB.187.12.4286-4289.2005, 1151709, 15937191.
22. Kyndt JA, Meyer TE, Cusanovich MA, Van Beeumen JJ. Characterization of a bacterial tyrosine ammonia lyase, a biosynthetic enzyme for the photoactive yellow protein. FEBS Lett 2002, 512:240-244. 10.1016/S0014-5793(02)02272-X, 11852088.
23. Rastogi N, Goh KS, Horgen L, Barrow WW. Synergistic activities of antituberculous drugs with cerulenin and trans-cinnamic acid against Mycobacterium tuberculosis. FEMS Immunol Med Microbiol 1998, 21:149-157. 10.1111/j.1574-695X.1998.tb01161.x, 9685005.
24. Chen YL, Huang ST, Sun FM, Chiang YL, Chiang CJ, Tsai CM, Weng CJ. Transformation of cinnamic acid from trans- to cis-form raises a notable bactericidal and synergistic activity against multiple-drug resistant Mycobacterium tuberculosis. Eur J Pharm Sci 2011, 43:188-194. 10.1016/j.ejps.2011.04.012, 21536127.
25. Patten CL, Glick BR. Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 1996, 42:207-220. 10.1139/m96-032, 8868227.
26. Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 2011, 39:W339-W346. 10.1093/nar/gkr466, 3125804, 21672958.
27. Blodgett JA, Oh DC, Cao S, Currie CR, Kolter R, Clardy J. Common biosynthetic origins for polycyclic tetramate macrolactams from phylogenetically diverse bacteria. Proc Natl Acad Sci USA 2010, 107:11692-11697. 10.1073/pnas.1001513107, 2900643, 20547882.
28. Hoster F, Schmitz JE, Daniel R. Enrichment of chitinolytic microorganisms: isolation and characterization of a chitinase exhibiting antifungal activity against phytopathogenic fungi from a novel Streptomyces strain. Appl Microbiol Biotechnol 2005, 66:434-442. 10.1007/s00253-004-1664-9, 15290142.
29. Lam YW, Wang HX, Ng TB. A robust cysteine-deficient chitinase-like antifungal protein from inner shoots of the edible chive Allium tuberosum. Biochem Biophys Res Commun 2000, 279:74-80. 10.1006/bbrc.2000.3821, 11112420.
30. Funkhouser JD, Aronson NN. Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evol Biol 2007, 7:96. 10.1186/1471-2148-7-96, 1945033, 17594485.
31. Kawase T, Saito A, Sato T, Kanai R, Fujii T, Nikaidou N, Miyashita K, Watanabe T. Distribution and phylogenetic analysis of family 19 chitinases in Actinobacteria. Appl Environ Microbiol 2004, 70:1135-1144. 10.1128/AEM.70.2.1135-1144.2004, 348904, 14766598.
32. Chang WT, Chen CS, Wang SL. An antifungal chitinase produced by Bacillus cereus with shrimp and crab shell powder as a carbon source. Curr Microbiol 2003, 47:102-108. 10.1007/s00284-002-3955-7, 14506855.
33. Wang SL, Chang WT. Purification and characterization of two bifunctional chitinases/lysozymes extracellularly produced by Pseudomonas aeruginosa K-187 in a shrimp and crab shell powder medium. Appl Environ Microbiol 1997, 63:380-386. 168330, 9023918.
34. Galloway WR, Hodgkinson JT, Bowden SD, Welch M, Spring DR. Quorum sensing in Gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem Rev 2011, 111:28-67. 10.1021/cr100109t, 21182299.
35. Williams P, Winzer K, Chan WC, Camara M. Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 2007, 362:1119-1134. 10.1098/rstb.2007.2039, 2435577, 17360280.
36. Sperandio V, Torres AG, Kaper JB. Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 2002, 43:809-821. 10.1046/j.1365-2958.2002.02803.x, 11929534.
37. Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 2001, 411:813-817. 10.1038/35081101, 11459062.
38. Uroz S, Dessaux Y, Oger P. Quorum sensing and quorum quenching: the yin and yang of bacterial communication. Chembiochem 2009, 10:205-216. 10.1002/cbic.200800521, 19072824.
39. Sio CF, Otten LG, Cool RH, Diggle SP, Braun PG, Bos R, Daykin M, Camara M, Williams P, Quax WJ. Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 2006, 74:1673-1682. 10.1128/IAI.74.3.1673-1682.2006, 1418629, 16495538.
40. Huang JJ, Petersen A, Whiteley M, Leadbetter JR. Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 2006, 72:1190-1197. 10.1128/AEM.72.2.1190-1197.2006, 1392938, 16461666.
41. Stock JB, Ninfa AJ, Stock AM. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev 1989, 53:450-490. 372749, 2556636.
42. Crepin S, Chekabab SM, Le Bihan G, Bertrand N, Dozois CM, Harel J. The Pho regulon and the pathogenesis of Escherichia coli. Vet Microbiol 2011, 153:82-88. 10.1016/j.vetmic.2011.05.043, 21700403.
43. Hsieh YJ, Wanner BL. Global regulation by the seven-component Pi signaling system. Curr Opin Microbiol 2010, 13:198-203. 10.1016/j.mib.2010.01.014, 2847643, 20171928.
44. Willsky GR, Malamy MH. Characterization of two genetically separable inorganic phosphate transport systems in Escherichia coli. J Bacteriol 1980, 144:356-365. 294655, 6998957.
45. Sola-Landa A, Moura RS, Martin JF. The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci USA 2003, 100:6133-6138. 10.1073/pnas.0931429100, 156338, 12730372.
46. Chae HZ, Robison K, Poole LB, Church G, Storz G, Rhee SG. Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Proc Natl Acad Sci USA 1994, 91:7017-7021. 10.1073/pnas.91.15.7017, 44329, 8041738.
47. Loschi L, Brokx S, Hills T, Zhang G, Bertero M, Lovering A, Weiner J, Strynadka N. Structural and biochemical identification of a novel bacterial oxidoreductase. J Biol Chem 2004, 279:50391-50400. 10.1074/jbc.M408876200, 15355966.
48. Cooksey DA. Copper uptake and resistance in bacteria. Mol Microbiol 1993, 7:1-5. 10.1111/j.1365-2958.1993.tb01091.x, 8437513.
49. Fong ST, Camakaris J, Lee BT. Molecular genetics of a chromosomal locus involved in copper tolerance in Escherichia coli K-12. Mol Microbiol 1995, 15:1127-1137. 10.1111/j.1365-2958.1995.tb02286.x, 7623666.
50. Chilcott GS, Hughes KT. Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol Mol Biol Rev 2000, 64:694-708. 10.1128/MMBR.64.4.694-708.2000, 99010, 11104815.
51. Gillen KL, Hughes KT. Molecular characterization of flgM, a gene encoding a negative regulator of flagellin synthesis in Salmonella typhimurium. J Bacteriol 1991, 173:6453-6459. 208980, 1655712.
52. Liu X, Matsumura P. The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J Bacteriol 1994, 176:7345-7351. 197124, 7961507.
53. Pruss BM, Matsumura P. A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division. J Bacteriol 1996, 178:668-674. 177710, 8550498.
54. Spangenberg C, Fislage R, Sierralta W, Tummler B, Romling U. Comparison of type IV-pilin genes of Pseudomonas aeruginosa of various habitats has uncovered a novel unusual sequence. FEMS Microbiol Lett 1995, 125:265-273. 10.1111/j.1574-6968.1995.tb07367.x, 7875574.
55. Craig L, Taylor RK, Pique ME, Adair BD, Arvai AS, Singh M, Lloyd SJ, Shin DS, Getzoff ED, Yeager M, et al. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 2003, 11:1139-1150. 10.1016/S1097-2765(03)00170-9, 12769840.
56. Baynham PJ, Ramsey DM, Gvozdyev BV, Cordonnier EM, Wozniak DJ. The Pseudomonas aeruginosa ribbon-helix-helix DNA-binding protein AlgZ (AmrZ) controls twitching motility and biogenesis of type IV pili. J Bacteriol 2006, 188:132-140. 10.1128/JB.188.1.132-140.2006, 1317580, 16352829.
57. Bingle LE, Bailey CM, Pallen MJ. Type VI secretion: a beginner's guide. Curr Opin Microbiol 2008, 11:3-8. 10.1016/j.mib.2008.01.006, 18289922.
58. Jani AJ, Cotter PA. Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 2010, 8:2-6. 10.1016/j.chom.2010.06.012, 2913581, 20638635.
59. Hayes JD, Wolf CR. Molecular mechanisms of drug resistance. Biochem J 1990, 272:281-295. 1149697, 1980062.
60. Neu HC. The crisis in antibiotic resistance. Science 1992, 257:1064-1073. 10.1126/science.257.5073.1064, 1509257.
61. Davies J. Inactivation of antibiotics and the dissemination of resistance genes. Science 1994, 264:375-382. 10.1126/science.8153624, 8153624.
62. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 2003, 67:593-656. 10.1128/MMBR.67.4.593-656.2003, 309051, 14665678.
63. Levy SB. Active efflux mechanisms for antimicrobial resistance. Antimicrob Agents Chemother 1992, 36:695-703. 10.1128/AAC.36.4.695, 189356, 1503431.
64. Nikaido H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 1994, 264:382-388. 10.1126/science.8153625, 8153625.
65. Linton KJ, Cooper HN, Hunter IS, Leadlay PF. An ABC-transporter from Streptomyces longisporoflavus confers resistance to the polyether-ionophore antibiotic tetronasin. Mol Microbiol 1994, 11:777-785. 10.1111/j.1365-2958.1994.tb00355.x, 8196549.
66. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K. Short protocols in molecular biology: a compendium of methods from current protocols in molecular biology 1995, New York, USA: Wiley, 3.
67. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome research 2010, 20:265-272. 10.1101/gr.097261.109, 2813482, 20019144.
68. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23:673-679. 10.1093/bioinformatics/btm009, 2387122, 17237039.
69. Tarailo-Graovac M, Chen N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinform 2009, 25:4.10.11-14.10.14.
70. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27:573-580. 10.1093/nar/27.2.573, 148217, 9862982.
71. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
72. Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 1999, 27:29-34. 10.1093/nar/27.1.29, 148090, 9847135.
73. Tatusov RL, Koonin EV, Lipman DJ. A genomic perspective on protein families. Science 1997, 278:631-637. 10.1126/science.278.5338.631, 9381173.
74. Pruitt KD, Tatusova T, Maglott DR. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 2007, 35:D61-D65. 10.1093/nar/gkl842, 1716718, 17130148.
75. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22:4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
76. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786. 10.1038/nmeth.1701, 21959131.
77. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, et al. CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 2011, 39:D225-D229. 10.1093/nar/gkq1189, 3013737, 21109532.
78. Someya N, Morohoshi T, Okano N, Otsu E, Usuki K, Sayama M, Sekiguchi H, Ikeda T, Ishida S. Distribution of N-acylhomoserine lactone-producing fluorescent pseudomonads in the phyllosphere and rhizosphere of potato (Solanum tuberosum L.). Microbes Environ 2009, 24:305-314. 10.1264/jsme2.ME09155, 21566390.
79. He Y, Xu T, Fossheim LE, Zhang XH. FliC, a flagellin protein, is essential for the growth and virulence of fish pathogen Edwardsiella tarda. PLoS One 2012, 7:e45070. 10.1371/journal.pone.0045070, 3443227, 23024793.
80. Hsu S, Lockwood J. Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl Microbiol 1975, 29:422-426. 186990, 234719.