Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Wilkinson, Paul ^a   Waterfield, Nicholas R ^b   Crossman, Lisa ^c   Corton, Craig ^c   Sanchez Contreras, Maria ^b   Vlisidou, Isabella ^b   Barron, Andrew ^c   Bignell, Alexandra ^c   Clark, Louise ^c   Ormond, Douglas ^c   Mayho, Matthew ^c   Bason, Nathalie ^c   Smith, Frances ^c   Simmonds, Mark ^c   Churcher, Carol ^c   Harris, David ^c   Thompson, Nicholas R ^c   Quail, Michael ^c   Parkhill, Julian ^c   Ffrench Constant, Richard H ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b University of Bath   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAQUINONE; BACTERIOCIN; CARBAPENEM; DNA; INSECT VENOM; PANTETHEINE PHOSPHATE; POLYKETIDE SYNTHASE; TRANSFER RNA; BACTERIAL DNA;

AGED; ARTICLE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL VIRULENCE; CASE REPORT; CHROMOSOME SIZE; CONSERVATION GENETICS; CONTROLLED STUDY; DISEASE CARRIER; ENTOMOPATHOGENY; FEMALE; GENE CASSETTE; GENE EXPRESSION; GENE LOCUS; GENE SEQUENCE; GENETIC CODE; GENETIC VARIABILITY; GENOME ANALYSIS; GENOME SIZE; GEOGRAPHICAL VARIATION (SPECIES); HUMAN; IMMUNE SYSTEM; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENICITY; PHOTORHABDUS; PHOTORHABDUS ASYMBIOTICA; PHOTORHABDUS LUMINESCENS; PLASMID; SPECIES COMPARISON; SYNTENY; TRINIDAD AND TOBAGO; TYPE III SECRETION SYSTEM; UNITED STATES; ANIMAL; CELL LINE; COMMUNICABLE DISEASE; COMPARATIVE GENOMIC HYBRIDIZATION; DNA SEQUENCE; ENTEROBACTERIACEAE INFECTION; GENETICS; GENOMIC ISLAND; GENOMICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOTH; MOUSE; SPECIES DIFFERENCE; VIRULENCE;

HEXAPODA; NEGIBACTERIA; PHOTORHABDUS; PHOTORHABDUS ASYMBIOTICA; PHOTORHABDUS LUMINESCENS; YERSINIA PESTIS;

ANIMALS; CELL LINE; COMMUNICABLE DISEASES, EMERGING; COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; ENTEROBACTERIACEAE INFECTIONS; GENOME, BACTERIAL; GENOMIC ISLANDS; GENOMICS; HUMANS; MICE; MOTHS; NORTH AMERICA; PHOTORHABDUS; PLASMIDS; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; VIRULENCE;

EID: 68349096343     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-302     Document Type: Article

References (78)

1. Yu Y Kim HS Chua HH Lin CH Sim SH Lin D Derr A Engels R DeShazer D Birren B et al Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis BMC Microbiol 2006, 6:46 1508146 16725056
2. Parkhill J Wren BW Thomson NR Titball RW Holden MT Prentice MB Sebaihia M James KD Churcher C Mungall KL et al Genome sequence of Yersinia pestis, the causative agent of plague Nature 2001, 413(6855):523-527 11586360
3. Waterfield NR Wren BW ffrench-Constant RH Invertebrates as a source of emerging human pathogens Nature Reviews Microbiology 2004, 2(10):833-841 15378047
4. Forst S Dowds B Boemare N Stackebrandt E Xenorhabdus and Photorhabdus spp.: Bugs that kill bugs Annu Rev Microbiol 1997, 51:47-72 9343343
5. Farmer JJ 3rd Jorgensen JH Grimont PA Akhurst RJ Poinar GO Jr Ageron E Pierce GV Smith JA Carter GP Wilson KL et al Xenorhabdus luminescens (DNA hybridization group 5) from human clinical specimens J Clin Microbiol 1989, 27(7):1594-1600 267621 2768446
6. Gerrard J Waterfield N Vohra R ffrench-Constant R Human infection with Photorhabdus asymbiotica: An emerging bacterial pathogen Microbes Infect 2004, 6(2):229-237 15049334
7. Heermann R Fuchs TM Comparative analysis of the Photorhabdus luminescens and the Yersinia enterocolitica genomes: Uncovering candidate genes involved in insect pathogenicity BMC Genomics 2008, 9:40 2266911 18221513
8. Ciche TA Kim KS Kaufmann-Daszczuk B Nguyen KC Hall DH Cell invasion and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes Appl Environ Microbiol 2008 74(8):2275-2287 2293164 18281425
9. Ciche TA Ensign JC For the insect pathogen Photorhabdus luminescens, which end of a nematode is out? Appl Environ Microbiol 2003, 69(4):1890-1897 154793 12676661
10. Hallem EA Rengarajan M Ciche TA Sternberg PW Nematodes, bacteria, and flies: A tripartite model for nematode parasitism Curr Biol 2007, 17(10):898-904 17475494
11. ffrench-Constant RH Eleftherianos I Reynolds SE A nematode symbiont sheds light on invertebrate immunity Trends Parasitol 2007, 23(11):514-517 17964855
12. ffrench-Constant RH Dowling A Waterfield NR Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture Toxicon 2007, 49(4):436-451 17207509
13. ffrench-Constant R Waterfield N Daborn P Joyce S Bennett H Au C Dowling A Boundy S Reynolds S Clarke D Photorhabdus: Towards a functional genomic analysis of a symbiont and pathogen FEMS Microbiol Rev 2003, 26(5):433-456 12586390
14. Forst S Nealson K Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp Microbiol Rev 1996, 60(1):21-43 239416 8852894
15. Gerrard JG Joyce SA Clarke DJ ffrench-Constant RH Nimmo GR Looke DF Feil EJ Pearce L Waterfield NR Nematode symbiont for Photorhabdus asymbiotica Emerg Infect Dis 2006, 12(10):1562-1564 17176572
16. Duchaud E Rusniok C Frangeul L Buchrieser C Givaudan A Taourit S Bocs S Boursaux-Eude C Chandler M Charles JF et al The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens Nat Biotechnol 2003, 21(11):1307-1313 14528314
17. Hinnebusch BJ The evolution of flea-borne transmission in Yersinia pestis Curr Issues Mol Biol 2005, 7(2):197-212 16053250
18. Mullikin JC Ning Z The phusion assembler Genome Res 2003, 13(1):81-90 430959 12529309
19. Berriman M Rutherford K Viewing and annotating sequence data with Artemis Brief Bioinform 2003, 4(2):124-132 12846394
20. ffrench-Constant R Waterfield N An ABC Guide to the Bacterial Toxin Complexes Adv Appl Microbiol 2005, 58C:169-183 16543033
21. Bowen D Rocheleau TA Blackburn M Andreev O Golubeva E Bhartia R ffrench-Constant RH Insecticidal toxins from the bacterium Photorhabdus luminescens Science 1998, 280(5372):2129-2132 9641921
22. Marokhazi J Waterfield N LeGoff G Feil E Stabler R Hinds J Fodor A ffrench-Constant RH Using a DNA microarray to investigate the distribution of insect virulence factors in strains of photorhabdus bacteria J Bacteriol 2003, 185(15):4648-4656 165762 12867479
23. Waterfield NR Bowen DJ Fetherston JD Perry RD ffrench-Constant RH The tc genes of Photorhabdus: A growing family Trends Microbiol 2001, 9(4):185-191 11286884
24. Silva CP Waterfield NR Daborn PJ Dean P Chilver T Au CP Sharma S Potter U Reynolds SE ffrench-Constant RH Bacterial infection of a model insect: Photorhabdus luminescens and Manduca sexta Cell Microbiol 2002, 4(6):329-339 12067318
25. Hares MC Hinchliffe SJ Strong PC Eleftherianos I Dowling AJ Ffrench-Constant RH Waterfield N The Yersinia pseudotuberculosis and Yersinia pestis toxin complex is active against cultured mammalian cells Microbiology 2008, 154(Pt 11):3503-3517 18957603
26. Yang G Dowling AJ Gerike U ffrench-Constant RH Waterfield NR Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth J Bacteriol 2006, 188(6):2254-2261 1428146 16513755
27. Hurst MR Glare TR Jackson TA Cloning Serratia entomophila antifeeding genes - a putative defective prophage active against the grass grub Costelytra zealandica J Bacteriol 2004, 186(15):5116-5128 451664 15262948
28. Daborn PJ Waterfield N Silva CP Au CPY Sharma S ffrench-Constant RH A single Photorhabdus gene makes caterpillars floppy (mcf) allows Esherichia coli to persist within and kill insects Proc Natl Acad Sci U S A 2002, 99(16):10742-10747 125031 12136122
29. Waterfield NR Daborn PJ Dowling AJ Yang G Hares M ffrench-Constant RH The insecticidal toxin Makes caterpillars floppy 2 (Mcf2) shows similarity to HrmA, an avirulence protein from a plant pathogen FEMS Microbiol Lett 2003, 229(2):265-270 14680709
30. Sicard M Hering S Schulte R Gaudriault S Schulenburg H The effect of Photorhabdus luminescens (Enterobacteriaceae) on the survival, development, reproduction and behaviour of Caenorhabditis elegans (Nematoda: Rhabditidae) Environ Microbiol 2007, 9(1):12-25 17227408
31. Waterfield N Kamita SG Hammock BD ffrench-Constant R The Photorhabdus Pir toxins are similar to a developmentally regulated insect protein but show no juvenile hormone esterase activity FEMS Microbiol Lett 2005, 245(1):47-52 15796978
32. Eleftherianos I Millichap PJ ffrench-Constant RH Reynolds SE RNAi suppression of recognition protein mediated immune responses in the tobacco hornworm Manduca sexta causes increased susceptibility to the insect pathogen Photorhabdus Dev Comp Immunol 2006, 30(12):1099-1107 16620974
33. ten Bokum AM Movahedzadeh F Frita R Bancroft GJ Stoker NG The case for hypervirulence through gene deletion in Mycobacterium tuberculosis Trends Microbiol 2008, 16(9):436-441 18701293
34. Brugirard-Ricaud K Duchaud E Givaudan A Girard PA Kunst F Boemare N Brehelin M Zumbihl R Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization Cell Microbiol 2005, 7(3):363-371 15679839
35. Brugirard-Ricaud K Givaudan A Parkhill J Boemare N Kunst F Zumbihl R Duchaud E Variation in the effectors of the type III secretion system among Photorhabdus species as revealed by genomic analysis J Bacteriol 2004, 186(13):4376-4381 421592 15205440
36. Finck-Barbancon V Goranson J Zhu L Sawa T Wiener-Kronish JP Fleiszig SM Wu C Mende-Mueller L Frank DW ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury Mol Microbiol 1997, 25(3):547-557 9302017
37. Matz C Moreno AM Alhede M Manefield M Hauser AR Givskov M Kjelleberg S Pseudomonas aeruginosa uses type III secretion system to kill biofilm-associated amoebae Isme J 2008, 2(8):843-852 18480848
38. Abd H Wretlind B Saeed A Idsund E Hultenby K Sandstrom G Pseudomonas aeruginosa utilises its type III secretion system to kill the free-living amoeba Acanthamoeba castellanii J Eukaryot Microbiol 2008, 55(3):235-243 18460161
39. Bakowski M Braun V Brumell JH Salmonella-containing vacuoles: Directing traffic and nesting to grow Traffic 2008, 9(12):2022-2031 18778407
40. Gerrard J Waterfield N Vohra R ffrench-Constant R Human infection with Photorhabdus asymbiotica: An emerging bacterial pathogen Microbes Infect 2004, 6(2):229-237 15049334
41. Park KS Ono T Rokuda M Jang MH Okada K Iida T Honda T Functional characterization of two type III secretion systems of Vibrio parahaemolyticus Infect Immun 2004, 72(11):6659-6665 523034 15501799
42. Hautefort I Thompson A Eriksson-Ygberg S Parker ML Lucchini S Danino V Bongaerts RJ Ahmad N Rhen M Hinton JC During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems Cell Microbiol 2008, 10(4):958-984 2343689 18031307
43. Chalabaev S Turlin E Charles JF Namane A Pages S Givaudan A Brito-Fravallo E Danchin A Biville F The HcaR regulatory protein of Photorhabdus luminescens affects the production of proteins involved in oxidative stress and toxemia Proteomics 2007, 7(24):4499-4510 18072208
44. Eleftherianos I Marokhazi J Millichap PJ Hodgkinson AJ Sriboonlert A ffrench-Constant RH Reynolds SE Prior infection of Manduca sexta with non-pathogenic Escherichia coli elicits immunity to pathogenic Photorhabdus luminescens: Roles of immune-related proteins shown by RNA interference Insect Biochem Mol Biol 2006, 36(6):517-525 16731347
45. Clarke DJ Photorhabdus: A model for the analysis of pathogenicity and mutualism Cell Microbiol 2008, 10(11):2159-2167 18647173
46. Raetz CR Reynolds CM Trent MS Bishop RE Lipid A modification systems in gram-negative bacteria Annu Rev Biochem 2007, 76:295-329 2569861 17362200
47. Derzelle S Turlin E Duchaud E Pages S Kunst F Givaudan A Danchin A The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects J Bacteriol 2004, 186(5):1270-1279 344422 14973084
48. Silva CP Waterfield NR Daborn PJ Dean P Chilver T Au CPY Sharma S Potter U Reynolds SE ffrench-Constant RH Bacterial infection of a model insect: Photorhabdus luminescens and Manduca sexta Cell Microbiol 2002, 4(6):329-339 12067318
49. Kim Y Ji D Cho S Park Y Two groups of entomopathogenic bacteria, Photorhabdus and Xenorhabdus, share an inhibitory action against phospholipase A2 to induce host immunodepression J Invertebr Pathol 2005, 89(3):258-264 15979640
50. Merchant D Ertl RL Rennard SI Stanley DW Miller JS Eicosanoids mediate insect hemocyte migration J Insect Physiol 2008, 54(1):215-221 17996890
51. Derzelle S Duchaud E Kunst F Danchin A Bertin P Identification, characterization, and regulation of a cluster of genes Involved in carbapenem biosynthesis in Photorhabdus luminescens Appl Environ Microbiol 2002, 68(8):3780-3789 124005 12147472
52. Brachmann AO Joyce SA Jenke-Kodama H Schwar G Clarke DJ Bode HB A type II polyketide synthase is responsible for anthraquinone biosynthesis in Photorhabdus luminescens Chembiochem 2007, 8(14):1721-1728 17722122
53. Joyce SA Brachmann AO Glazer I Lango L Schwar G Clarke DJ Bode HB Bacterial biosynthesis of a multipotent stilbene Angewantde Chemie 2008, 47:1942-1945
54. Ciche TA Bintrim SB Horswill AR Ensign JC A Phosphopantetheinyl transferase homolog is essential for Photorhabdus luminescens to support growth and reproduction of the entomopathogenic nematode Heterorhabditis bacteriophora J Bacteriol 2001,183(10):3117-3126 95212 11325940
55. Waterfield NR Sanchez-Contreras M Eleftherianos I Dowling A Wilkinson P Parkhill J Thomson N Reynolds SE Bode HB Dorus S et al Rapid Virulence Annotation (RVA): Identification of virulence factors using a bacterial genome library and multiple invertebrate hosts Proc Natl Acad Sci USA 2008, 105(41):15967-15972 2572985 18838673
56. Sharma S Waterfield N Bowen D Rocheleau T Holland L James R ffrench-Constant R The lumicins: Novel bacteriocins from Photorhabdus luminescens with similarity to the uropathogenic-specific protein (USP) from uropathogenic Escherichia coli FEMS Microbiol Lett 2002, 214(2):241-249 12351238
57. Gaudriault S Thaler JO Duchaud E Kunst F Boemare N Givaudan A Identification of a P2-related prophage remnant locus of Photorhabdus luminescens encoding an R-type phage tail-like particle FEMS Microbiol Lett 2004, 233(2):223-231 15063490
58. Waterfield NR Daborn PJ ffrench-Constant RH Genomic islands in Photorhabdus Trends Microbiol 2002, 10(12):541-545 12564983
59. Gaudriault S Duchaud E Lanois A Canoy AS Bourot S Derose R Kunst F Boemare N Givaudan A Whole-genome comparison between Photorhabdus strains to identify genomic regions involved in the specificity of nematode interaction J Bacteriol 2006, 188(2):809-814 1347316 16385072
60. Bennett HP Clarke DJ The pbgPE operon in Photorhabdus luminescens is required for pathogenicity and symbiosis J Bacteriol 2005, 187(1):77-84 538804 15601690
61. Bartra SS Styer KL O'Bryant DM Nilles ML Hinnebusch BJ Aballay A Plano GV Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer membrane protein Infect Immun 2008, 76(2):612-622 2223467 18025094
62. Fischer-Le Saux M Viallard V Brunel B Normand P Boemare NE Polyphasic classification of the genus Photorhabdus and proposal of new taxa: P. luminescens subsp. luminescens subsp. nov., P. luminescens subsp. akhurstii subsp. nov., P. luminescens subsp. laumondii subsp. nov., P. temperata sp. nov., P. temperata subsp. temperata subsp. nov. and P. asymbiotica sp. nov Int J Syst Bacteriol 1999, 49(Pt 4):1645-1656 10555346
63. Kuwata R Yoshiga T Yoshida M Kondo E Mutualistic association of Photorhabdus asymbiotica with Japanese heterorhabditid entomopathogenic nematodes Microbes Infect 2008, 10(7):734-741 18538616
64. Tounsi S Blight M Jaoua S de Lima Pimenta A From insects to human hosts: Identification of major genomic differences between entomopathogenic strains of Photorhabdus and the emerging human pathogen Photorhabdus asymbiotica Int J Med Microbiol 2006, 296(8):521-530 17029962
65. Liu D Burton S Glancy T Li ZS Hampton R Meade T Merlo DJ Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana Nat Biotechnol 2003, 21:1307-1313 14528314
66. Zhao R Han R Qiu X Yan X Cao L Liu X Cloning and heterologous expression of insecticidal genes from Photorhabdus luminescens TT01 in Enterobacter cloacae for termite control Appl Environ Microbiol 2008, 74(23):7219-7226 2592930 18836027
67. Bondi M Messi P Sabia C Baccarani Contri M Manicardi G Antimicrobial properties and morphological characteristics of two Photorhabdus luminescens strains New Microbiol 1999, 22(2):117-127 10322611
68. Costa SC Girard PA Brehelin M Zumbihl R The emerging human pathogen Photorhabdus asymbiotica is a facultative intracellular bacterium and induces apoptosis of macrophage-like cells Infect Immun 2009, 77(3):1022-1030 19075024
69. Dowling AJ Daborn PJ Waterfield NR Wang P Streuli CH ffrench-Constant RH The insecticidal toxin Makes caterpillars floppy (Mcf) promotes apoptosis in mammalian cells Cell Microbiol 2004, 6(4):345-353 15009026
70. Justice SS Hunstad DA Seed PC Hultgren SJ Filamentation by Escherichia coli subverts innate defenses during urinary tract infection Proc Natl Acad Sci USA 2006, 103(52):19884-19889 1750882 17172451
71. Reckseidler-Zenteno SL DeVinney R Woods DE The capsular polysaccharide of Burkholderia pseudomallei contributes to survival in serum by reducing complement factor C3b deposition Infect Immun 2005, 73(2):1106-1115 547107 15664954
72. Altstchul S Gish W Miller W Myers E Lipman D Basic local alignment search tool Journal of Molecular Biology 1990, 215:403-410 2231712
73. Frishman D Mironov A Mewes HW Gelfand M Combining diverse evidence for gene recognition in completely sequenced bacterial genomes Nucleic Acids Res 1998, 26(12):2941-2947 147632 9611239
74. Delcher AL Harmon D Kasif S White O Salzberg SL Improved microbial gene identification with GLIMMER Nucleic Acids Res 1999, 27(23):4636-4641 148753 10556321
75. Bateman A Birney E Cerruti L Durbin R Etwiller L Eddy SR Griffiths-Jones S Howe KL Marshall M Sonnhammer EL The Pfam protein families database Nucleic Acids Res 2002, 30(1):276-280 99071 11752314
76. Rutherford K Parkhill J Crook J Horsnell T Rice P Rajandream MA Barrell B Artemis: Sequence visualization and annotation Bioinformatics 2000, 16(10):944-945 11120685
77. Griffiths-Jones S Bateman A Marshall M Khanna A Eddy SR Rfam: An RNA family database Nucleic Acids Res 2003, 31(1):439-441 165453 12520045
78. Turlin E Pascal G Rousselle JC Lenormand P Ngo S Danchin A Derzelle S Proteome analysis of the phenotypic variation process in Photorhabdus luminescens Proteomics 2006, 6(9):2705-2725 16548063