Phylogenetic analysis of a gene cluster encoding an additional, rhizobial-like type III secretion system that is narrowly distributed among Pseudomonas syringae strains

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Gazi, Anastasia D ^a,b,c   Sarris, Panagiotis F ^a,d   Fadouloglou, Vasiliki E ^a,e   Charova, Spyridoula N ^a   Mathioudakis, Nikolaos ^a   Panopoulos, Nicholas J ^a   Kokkinidis, Michael ^a,b  

^a UNIVERSITY OF CRETE   (Greece)

^b INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF CRETE   (Greece)

^e DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

Author keywords

Common ancestry; Evolutionary relationships; Gene organization; Horizontal transfer events; Hrc1Type III secretion system; Pathogenicity; Phylogenetic analysis; Pseudomonas syringae; Rhizobium Type III secretion system; RT PCR

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; COMPUTER MODEL; GENE CLUSTER; NONHUMAN; PHYLOGENETIC TREE; PSEUDOMONAS SYRINGAE; REAL TIME POLYMERASE CHAIN REACTION; RHIZOBIALES; RHIZOBIUM; TYPE III SECRETION SYSTEM;

BACTERIAL SECRETION SYSTEMS; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE ORDER; GENE TRANSFER, HORIZONTAL; MULTIGENE FAMILY; PHYLOGENY; PLASMIDS; PSEUDOMONAS SYRINGAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHIZOBIUM; SYNTENY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS SYRINGAE; RHIZOBIUM; RHIZOBIUM SP.;

EID: 84865566722     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-188     Document Type: Article

References (65)

1. Secretion by numbers: protein traffic in prokaryotes. Economou A, Christie PJ, Fernandez RC, Palmer T, Plano GV, Pugsley AP, Mol Microbiol 2006 62 2 308 319 10.1111/j.1365-2958.2006.05377.x 17020575 (Pubitemid 44477223)
2. Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. Tseng T-T, Tyler BM, Setubal JC, BMC Microbiol 2009 9 Suppl 1 2 10.1186/1471-2180-1189-S1181-S1182 19278550
3. The versatile bacterial type IV secretion systems. Cascales E, Christie PJ, Nat Rev Microbiol 2003 1 2 137 149 10.1038/nrmicro753 15035043
4. The type III secretion injectisome. Cornelis GR, Nat Rev Microbiol 2006 4 811 825 10.1038/nrmicro1526 17041629 (Pubitemid 44593948)
5. Coiled-coils in type III secretion systems: structural flexibility, disorder and biological implications. Gazi AD, Charova SN, Panopoulos NJ, Kokkinidis M, Cell Microbiol 2009 11 5 719 729 10.1111/j.1462-5822.2009.01297.x 19215225
6. Playing the "Harp": evolution of our understanding of hrp/hrc Genes. Tampakaki AP, Skandalis N, Gazi AD, Bastaki MN, Sarris PF, Charova SN, Kokkinidis M, Panopoulos NJ, Annu Rev Phytopathol 2010 17 347 370
7. Conserved features of type III secretion. Tampakaki AP, Fadouloglou VE, Gazi AD, Panopoulos NJ, Kokkinidis M, Cell Microbiol 2004 6 9 805 816 10.1111/j.1462-5822.2004.00432.x 15272862 (Pubitemid 39162623)
8. Type III secretion: more systems than you think. Troisfontaines P, Cornelis GR, Physiol 2005 20 326 339 10.1152/physiol.00011.2005 (Pubitemid 41457398)
9. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gophna U, Ron EZ, Graur D, Gene 2003 312 151 163 12909351 (Pubitemid 37338120)
10. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Altschul SF, Madden TL, Schffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, Nucleic Acid Res 1997 25 17 3389 3402 10.1093/nar/25.17.3389 9254694 (Pubitemid 27359211)
11. FoldIndex©: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Prilusky J, Felder CE, Zeev-Ben Mordehai T, Rydberg EH, Man O, Beckmann JS, Silman IJ, Prilusky J, Felder CE, Zeev-Ben Mordehai T, Rydberg EH, Man O, Beckmann JS, Silman IJLS, Bioinf 2005 21 3435 3438 10.1093/bioinformatics/bti537 (Pubitemid 41222454)
12. Protein secondary structure prediction based on position-specific scoring matrices. Jones DT, J Mol Biol 1999 292 2 195 202 10.1006/jmbi.1999.3091 10493868 (Pubitemid 29435759)
13. Handbook Totowa, New Jersey: Humana Press 2005
14. Predicting coiled coils from protein sequences. Lupas A, Van Dyke M, Stock J, Science 1991 252 1162 1164 10.1126/science.252.5009.1162 17797907 (Pubitemid 21917026)
15. Identifying periodic occurences of a template with applications to protein structure. Fischetti VA, Landau GM, Schmidt JP, Sellers P, Inform Process Let 1993 45 11 18 10.1016/0020-0190(93)90245-5 (Pubitemid 23639501)
16. Enhanced genome annotation with structural profiles in the program 3D-PSSM. Kelley LA, MacCallum RM, Sternberg MJE, J Mol Biol 2000 299 499 500 10860755
17. The PSIPRED protein structure prediction server. McGuffin LJ, Bryson K, Jones DT, Bioinfor 2000 16 404 405 10.1093/bioinformatics/16.4.404 (Pubitemid 30417087)
18. DnaSP v5: A software for comprehensive analysis of DNA polymorhism data. Librado P, Rozas J, Bioinfor 2009 25 1451 1452 10.1093/bioinformatics/btp187
19. ClustalW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position, specific gap penalties, and weight matrix choice. Thompson JD, Higgins DG, Gibson TJ, Nucleic Acid Res 1994 22 4673 4680 10.1093/nar/22.22.4673 7984417 (Pubitemid 24354800)
20. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Saitou N, Nei M, Mol Biol Evol 1987 4 4 406 425 3447015
21. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Tamura K, Dudley J, Nei M, Kumar S, Mol Biol Evol 2007 24 1596 1599 10.1093/molbev/msm092 17488738 (Pubitemid 47236692)
22. Confidence limits on phylogenies: an approach using the bootstrap. Felsenstein J, Evolution 1985 39 4 783 791 10.2307/2408678
23. Zuckerkandl E, Pauling L, Evolutionary divergence and convergence in proteins New York: Academic 1965
24. Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. Rahme LG, Mindrinos MN, Panopoulos NJ, J Bacteriol 1992 174 11 3499 3507 1592805
25. Messenger RNA-based RT-PCR detection of viable Salmonella. Rijpensa N, Jannesb G, Hermana L, Intern Diary J 2002 12 233 238 10.1016/S0958-6946(01) 00158-3 (Pubitemid 34234399)
26. Type III protein secretion systems in bacterial pathogens of animals and plants. Hueck CJ, Microbiol Mol Biol Rev 1998 62 2 379 433 9618447 (Pubitemid 28270280)
27. A single promoter sequence recognized by a newly identified alternate sigma factor directs expression of pathogenicity and host range determinants in Pseudomonas syringae. Xiao Y, Hutcheson SW, J Bacteriol 1994 176 10 3089 3091 8188613 (Pubitemid 24152960)
28. Symbiotic implications of type III protein secretion machinery in Rhizobium. Viprey V, Del Greco A, Golinowski W, Broughton WJ, Perret X, Mol Microbiol 1998 28 6 1381 1389 10.1046/j.1365-2958.1998.00920.x 9680225 (Pubitemid 28293559)
29. Mutational and Transcriptional Analysis of the Type III Secretion System of Bradyrhizobium japonicum. Krause A, Doerfel A, Göttfert M, MPMI 2002 15 12 1228 1235 10.1094/MPMI.2002.15.12.1228 12481995 (Pubitemid 36003310)
30. Transcriptional organisation and expression of nolXWBTUV, a locus that regulates cultivar-specific nodulation of soybean by Rhizobium fredii USDA257. Kovács LG, Balatti PA, Krishnan HB, Pueppke SG, Mol Microbiol 1995 17 923 933 10.1111/j.1365-2958.1995.mmi-17050923.x 8596441
31. Structure of HrcQB-C, a concerved component of the bacterial type III secretion systems. Fadouloglou VE, Tampakaki AP, Glykos NM, Bastaki MN, Hadden JM, Phillips SE, Panopoulos NJ, Kokkinidis M, Proc Natl Acad Sci USA 2004 101 70 75 10.1073/pnas.0304579101 14694203 (Pubitemid 38084205)
32. On the quaternary association of the type III secretion system HrcQB-C protein: experimental evidence differentiates among the various oligomerization models. Fadouloglou VE, Bastaki MN, Ashcroft AE, Phillips SEV, Panopoulos NJ, Glykos NM, Kokkinidis M, J Struct Biol 2009 166 2 214 225 10.1016/j.jsb.2009.01. 008 19374021
33. Evidence for a coiled-coil interaction mode of disordered proteins from bacterial type III secretion systems. Gazi AD, Bastaki M, Charova SN, Gkougkoulia EA, Kapellios EA, Panopoulos NJ, Kokkinidis M, J Biol Chem 2008 283 49 34062 34068 10.1074/jbc.M803408200 18836182
34. Bioinformatics analysis of the locus for enterocyte effacement provides novel insights into type-III secretion. Pallen MJ, Beatson SA, Bailey CM, BMC Microbiol 2005 5 9 10.1186/1471-2180-5-9 15757514 (Pubitemid 40706096)
35. Molecular basis of symbiosis between Rhizobium and legumes. Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X, Nat 1997 387 394 401 10.1038/387394a0 (Pubitemid 27227203)
36. Rhizobium type III secretion systems: legume charmers or alarmers? Marie C, Broughton WJ, Deakin WJ, Curr Opin Plant Biol 2001 4 4 336 342 10.1016/S1369-5266(00)00182-5 11418344 (Pubitemid 32620717)
37. The mosaic structure of the symbiotic plasmid of Rhizobium etli CFN42 and its relation to other symbiotic genome compartments. González V, Bustos P, Ramírez-Romero MA, Medrano-Soto A, Salgado H, Hernández- González I, Hernández-Celis JC, Quintero V, Moreno-Hagelsieb G, Girard L, et al. Gen Biol 2003 4 6 36 10.1186/gb-2003-4-6-r36
38. Rhizobium sp. Strain NGR234 Possesses a Remarkable Number of Secretion Systems. Schmeisser C, Liesegang H, Krysciak D, Bakkou N, Le Quere A, Wollherr A, Heinemeyer I, Morgenstern B, Pommerening-Roser A, Flores M, et al. Appl Environ Microbiol 2009 75 12 4035 4045 10.1128/AEM.00515-09 19376903
39. The hrpK operon of Pseudomonas syringae pv. tomato DC3000 encodes two proteins secreted by the type III (Hrp) protein secretion system: HopB1 and HrpK, a putative type III translocator. Petnicki-Ocwiega T, van Dijk K, Alfano JR, J Bacteriol 2005 187 649 663 10.1128/JB.187.2.649-663.2005 15629936 (Pubitemid 40096252)
40. The Yersinia pestis YscY Protein Directly Binds YscX, a Secreted Component of the Type III Secretion Machinery. Day JB, Plano GV, J Bacteriol 2000 182 7 1834 1843 10.1128/JB.182.7.1834-1843.2000 10714987 (Pubitemid 30165369)
41. AAA + ATPases in the Initiation of DNA Replication. Duderstadt KE, Berger JM, Crit Rev Biochem Mol Biol 2008 43 163 187 10.1080/10409230802058296 18568846 (Pubitemid 351883154)
42. Tetratricopeptide-like repeats in type-III-secretion chaperones and regulators. Pallen MJ, Francis MS, Futterer K, FEMS Microbiol Lett 2003 223 53 60 10.1016/S0378-1097(03)00344-6 12799000 (Pubitemid 36694410)
43. Type III secretion chaperone-dependent regulation: activation of virulence genes by SicA and InvF in Salmonella typhimurium. Darwin KH, Miller VL, EMBO J 2001 20 1850 1862 10.1093/emboj/20.8.1850 11296219 (Pubitemid 32397388)
44. Whole-Genome Sequence Analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, Brinkac LM, Daugherty SC, DeBoy R, Durkin AS, Giglio MG, et al. J Bacteriol 2005 187 18 6488 6498 10.1128/JB.187.18.6488-6498.2005 16159782 (Pubitemid 41318408)
45. Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster. Sawada H, Suzuki F, Matsuda I, Saitou N, J Mol Evol 1999 49 627 644 10.1007/PL00006584 10552044 (Pubitemid 32268719)
46. The -proteobacteria: the Darwin finches of the bacterial world. Ettema TJG, Andersson SGE, Biol Lett 2009 5 391 393 10.1098/rsbl.2009.0227 19386649
47. Rhizobial secreted proteins as determinants of host specificity in the rhizobium-legume symbiosis. Fauvart M, Michiels J, FEMS Microbiol Lett 2008 285 1 9 10.1111/j.1574-6968.2008.01254.x 18616593 (Pubitemid 352000224)
48. Bacterial colonization of leaves: a spectrum of Strategies. Beattie GA, Lindow SE, Phytopathol 1999 89 5 353 359 10.1094/PHYTO.1999.89.5.353 (Pubitemid 29205838)
49. Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JH, Annu Rev Microbiol 2006 60 425 449 10.1146/annurev.micro.60.080805.142251 16753033 (Pubitemid 44627956)
50. Type III protein secretion systems in plant and animal pathogenic bacteria. He SY, Annu Rev Phytopathol 1998 36 363 392 10.1146/annurev.phyto.36. 1.363 15012505 (Pubitemid 28456413)
51. Bacteria in the Leaf Ecosystem with Emphasis on Pseudomonas syringae-a Pathogen, Ice Nucleus, and Epiphyte. Hirano SS, Upper CD, Microbiol Mol Biol Rev 2000 64 624 653 10.1128/MMBR.64.3.624-653.2000 10974129
52. Roadmap to new virulence determinants in Pseudomonas syringae: Insights from comparative genomics and genome organization. Lindeberg M, Myers CR, Collmer A, Schneider DJ, Mol Plant Microbiol Inter 2008 21 685 700 10.1094/MPMI-21-6-0685 (Pubitemid 351929163)
53. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LM, et al. Nature 2002 417 459 463 10.1038/417459a 12024217 (Pubitemid 34563540)
54. Comparative genome analysis provides insights into the evolution and adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. Green S, Studholme DJ, Laue BE, Dorati F, Lovell H, Arnold D, Cottrell JE, Bridgett S, Blaxter M, Huitema E, et al. PLoS One 2010 5 4 10224 10.1371/journal.pone. 0010224 20419105
55. Annotation and overview of the Pseudomonas savastanoi pv. savastanoi NCPPB 3335 draft genome reveals the virulence gene complement of a tumour-inducing pathogen of woody hosts. Rodríguez-Palenzuela P, Matas IM, Murillo J, López-Solanilla E, Bardaji L, Pérez-Martínez I, Rodríguez-Moskera ME, Penyalver R, López MM, Quesada J, et al. Environ Microbiol 2010 12 6 1604 1620 20370821
56. Genome sequence analyses of Pseudomonas savastanoi pv. glycinea and subtractive hybridization-based comparative genomics with nine pseudomonads. Qi M, Wang D, Bradley CA, Zhao Y, PLoS One 2011 6 1 16451 10.1371/journal.pone. 0016451 21304594
57. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Huynh TV, Dahlbeck D, Staskawicz BJ, Science 1989 245 4924 1374 1377 10.1126/science.2781284 2781284
58. Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc Locus are common leaf colonizers equipped with an atypical type III secretion system. Clarke CR, Cai R, Studholme DJ, Guttman DS, Vinatzer BA, Mol Plant Microbe Interact 2010 23 2 198 210 10.1094/MPMI-23-2-0198 20064063
59. Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. Records AR, Gross DC, J Bacteriol 2010 192 14 3584 3596 10.1128/JB.00114-10 20472799
60. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ, Nat Cell Biol 2007 9 7 797 803 10.1038/ncb1605 17558395 (Pubitemid 47019466)
61. Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Lesic B, Starkey M, He J, Hazan R, Rahme LG, Microbiology 2009 155 Pt 9 2845 2855 19497948
62. The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. He J, Baldini RL, Deziel E, Saucier M, Zhang Q, Liberati NT, Lee D, Urbach J, Goodman HM, Rahme LG, Proc Natl Acad Sci USA 2004 101 2530 2535 10.1073/pnas.0304622101 14983043 (Pubitemid 38269345)
63. Horizontal Gene Transfer Regulation in Bacteria as a β Spandrel β of DNA Repair Mechanisms. Fall S, Mercier A, Bertolla F, Calteau A, Gueguen L, Perŗi G, Vogel TM, Simonet P, PLoS One 2007 2 10 1055 10.1371/journal.pone.0001055 17957239 (Pubitemid 351552224)
64. Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Youssef YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, De Bruijn F, Stoltzfus J, Buckley D, et al. Plant Soil 1997 194 99 114 10.1023/A:1004269902246 (Pubitemid 27463647)
65. Rhizobium oryzae sp. nov., isolated from the wild rice Oryza alta. Peng G, Yuan Q, Li H, Zhang W, Tan Z, Int J Syst Evol Microbiol 2008 58 2158 2163 10.1099/ijs.0.65632-0 18768622