The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Chaston, John M ^a   Suen, Garret ^a   Tucker, Sarah L ^b   Andersen, Aaron W ^a   Bhasin, Archna ^c   Bode, Edna ^d   Bode, Helge B ^d   Brachmann, Alexander O ^d   Cowles, Charles E ^a   Cowles, Kimberly N ^a   Darby, Creg ^e   de Léon, Limaris ^a   Drace, Kevin ^f   Du, Zijin ^b   Givaudan, Alain ^g   Herbert Tran, Erin E ^a   Jewell, Kelsea A ^a   Knack, Jennifer J ^a   Krasomil Osterfeld, Karina C ^b   Kukor, Ryan ^a   Lanois, Anne ^g   Latreille, Phil ^b   Leimgruber, Nancy K ^b   Lipke, Carolyn M ^a   Liu, Renyi ^h   Lu, Xiaojun ^a   Martens, Eric C ⁱ   Marri, Pradeep R ^h   Médigue, Claudine ^j   Menard, Megan L ^a   Miller, Nancy M ^b   Morales Soto, Nydia ^k   Norton, Stacie ^b   Ogier, Jean Claude ^g   Orchard, Samantha S ^a   Park, Dongjin ^k   Park, Youngjin ^a   Qurollo, Barbara A ^b   Sugar, Darby Renneckar ^a   Richards, Gregory R ^a   Rouy, Zoé ^j   Slominski, Brad ^a   Slominski, Kathryn ^a   Snyder, Holly ^k   Tjaden, Brian C ^l   van der Hoeven, Ransome ^k   Welch, Roy D ^m   Wheeler, Cathy ⁿ   Xiang, Bosong ^b   Barbazuk, Brad ^o   Gaudriault, Sophie ^g   Goodner, Brad ⁿ   Slater, Steven C ^p   Forst, Steven ^k   Goldman, Barry S ^b   Goodrich Blair, Heidi ^a   more..

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b MONSANTO COMPANY   (United States)

^c VALDOSTA STATE UNIVERSITY   (United States)

^d GOETHE UNIVERSITY   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f MERCER UNIVERSITY   (United States)

^g UNIV MONTPELLIER   (France)

^h University of Arizona   (United States)

ⁱ UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^j CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^k UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^l WELLESLEY COLLEGE   (United States)

^m SYRACUSE UNIVERSITY   (United States)

ⁿ HIRAM COLLEGE   (United States)

^o UNIVERSITY OF FLORIDA   (United States)

^p USA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; TRANSFER RNA; BACTERIAL DNA;

ARTICLE; BACTERIAL GENOME; CONTROLLED STUDY; ENDOSYMBIONT; ENTOMOPATHOGENY; MICROBIAL DIVERSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORHABDUS; PHOTORHABDUS ASYMBIOTICA; PHOTORHABDUS LUMINESCENS; PHYLOGENY; SPECIES DIFFERENTIATION; XENORHABDUS; XENORHABDUS BOVIENII; XENORHABDUS NEMATOPHILA; ANIMAL; BACTERIAL CHROMOSOME; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; ENTEROBACTERIACEAE; GENETIC VARIABILITY; GENETICS; GENOMICS; HOST PARASITE INTERACTION; HOST PATHOGEN INTERACTION; INSECT; METHODOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; NEMATODE; PARASITOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE; SYMBIOSIS;

BACTERIA (MICROORGANISMS); HEXAPODA; NEMATODA; PHOTORHABDUS; PHOTORHABDUS ASYMBIOTICA; PHOTORHABDUS LUMINESCENS; XENORHABDUS; XENORHABDUS BOVIENII; XENORHABDUS NEMATOPHILA;

ANIMALS; CHROMOSOMES, BACTERIAL; DNA, BACTERIAL; ENTEROBACTERIACEAE; GENETIC VARIATION; GENOME, BACTERIAL; GENOMICS; HOST-PARASITE INTERACTIONS; HOST-PATHOGEN INTERACTIONS; INSECTS; MOLECULAR SEQUENCE DATA; NEMATODA; PHOTORHABDUS; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS; XENORHABDUS;

EID: 84859251997     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027909     Document Type: Article

References (128)

1. Spratt BG, Staley JT, Fischer MC, (2006) Introduction: species and speciation in microorganisms. Phil Trans Roy Soc B 361: 1897.
2. Konstantinidis KT, Tiedje JM, (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187: 6258-6264.
3. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, et al.(2006) Toward automatic reconstruction of a highly resolved tree of life. Science 311: 1283-1287.
4. Gupta RS, Griffiths E, (2002) Critical issues in bacterial phylogeny. Theor Popul Biol 61: 423-434.
5. Suen G, Goldman BS, Welch RD, (2007) Predicting prokaryotic ecological niches using genome sequence analysis. PLoS ONE 2: e743.
6. Wu H, Moore E, (2010) Association analysis of the general environmental conditions and prokaryotes' gene distributions in various functional groups. Genomics 96: 27-38.
7. Chaffron S, Rehrauer H, Pernthaler J, von Mering C, (2010) A global network of coexisting microbes from environmental and whole-genome sequence data. Genome Res 20: 947.
8. Moran NA, (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108: 583-586.
9. Ohno S, (1970) Evolution by Gene Duplication. New York Springer 160.
10. Woese CR, (1987) Bacterial evolution. Microbiol Rev 51: 221-271.
11. Ochman H, Lawrence JG, Groisman EA, (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.
12. Goodrich-Blair H, Clarke DJ, (2007) Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol 64: 260-268.
13. Griffin CT, O'Callaghan KM, Dix I, (2001) A self-fertile species of Steinernema from Indonesia: further evidence of convergent evolution amongst entomopathogenic nematodes? Parasitol 122: 181-186.
14. Poinar GO Jr, (1993) Origins and phylogenetic relationships of the entomophilic rhabditids, Heterorhabditis and Steinernema. Fund Appl Nematol 16: 333-338.
15. Poinar GO, (1966) The presence of Achromobacter nematophilus in the infective stage of a Neoaplectana sp. (Steinernematidae: Nematoda). Nematologica 12: 105-108.
16. Poinar GO, Thomas GM, (1967) The nature of Achromobacter nematophilus as an insect pathogen. J Invertebr Pathol 9: 510-514.
17. Thomas GM, Poinar GO, (1979) Xenorhabdus, new genus of entomopathogenic, nematophilic bacteria of the family Enterobacteriaceae. Int J Syst Bacteriol 29: 352-360.
18. Akhurst RJ, (1983) Taxonomic study of Xenorhabdus, a genus of bacteria symbiotically associated with insect pathogenic nematodes. Int J Syst Bacteriol 33: 38-45.
19. Forst S, Clarke D, (2002) Bacteria-nematode symbioses. In: Gaugler R, editors. Entomopathogenic Nematology Wallingford, UK CABI Publishing pp. 57-77.
20. Snyder H, Stock SP, Kim SK, Flores-Lara Y, Forst S, (2007) New insights into the colonization and release processes of Xenorhabdus nematophila and the morphology and ultrastructure of the bacterial receptacle of its nematode host, Steinernema carpocapsae. Appl Environ Microbiol 73: 5338-5346.
21. Bird AF, Akhurst RJ, (1983) The nature of the intestinal vesicle in nematodes of the family Steinernematidae. Int J Parasitol 13: 599-606.
22. Dunphy GB, Webster JM, (1988) Lipopolysaccharides of Xenorhabdus nematophilus (Enterobacteriaceae) and their haemocyte toxicity in non-immune Galleria mellonella (Insecta: Lepidoptera) larvae. J Gen Microbiol 134: 1017-1028.
23. Park D, Forst S, (2006) Co-regulation of motility, exoenzyme and antibiotic production by the EnvZ-OmpR-FlhDC-FliA pathway in Xenorhabdus nematophila. Mol Microbiol 61: 1397-1412.
24. Sergeant M, Baxter L, Jarrett P, Shaw E, Ousley M, et al.(2006) Identification, typing, and insecticidal activity of Xenorhabdus isolates from entomopathogenic nematodes in United Kingdom soil and characterization of the xpt toxin loci. Appl Environ Microbiol 72: 5895-5907.
25. Cowles KN, Cowles CE, Richards GR, Martens EC, Goodrich-Blair H, (2007) The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell Microbiol 9: 1311-1323.
26. Park Y, Herbert EE, Cowles CE, Cowles KN, Menard ML, et al.(2007) Clonal variation in Xenorhabdus nematophila virulence and suppression of Manduca sexta immunity. Cell Microbiol 9: 645-656.
27. Shrestha S, Kim Y, (2007) An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits hemocyte phagocytosis of Spodoptera exigua by inhibiting phospholipase A(2). J Invertebr Pathol 96: 64-70.
28. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, et al.(2004) GO::TermFinder--open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710-3715.
29. Cowles KN, Goodrich-Blair H, (2005) Expression and activity of a Xenorhabdus nematophila haemolysin required for full virulence towards Manduca sexta insects. Cell Microbiol 7: 209-219.
30. Chandra H, Khandelwal P, Khattri A, Banerjee N, (2008) Type 1 fimbriae of insecticidal bacterium Xenorhabdus nematophila is necessary for growth and colonization of its symbiotic host nematode Steinernema carpocapsae. Environ Microbiol 10: 1285-1295.
31. Vigneux F, Zumbihl R, Jubelin G, Ribeiro C, Poncet J, et al.(2007) The xaxAB genes encoding a new apoptotic toxin from the insect pathogen Xenorhabdus nematophila are present in plant and human pathogens. J Biol Chem 282: 9571-9580.
32. Caldas C, Cherqui A, Pereira A, Simoes N, (2002) Purification and characterization of an extracellular protease from Xenorhabdus nematophila involved in insect immunosuppression. Appl Environ Microbiol 68: 1297-1304.
33. Akhurst RJ, (1982) Antibiotic activity of Xenorhabdus spp., bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. J Gen Microbiol 128: 3061-3065.
34. Webster JM, Genhui C, Kaiji H, Li J, (2002) Bacterial metabolites. In: Gaugler R, editors. Entomopathogenic nematology New York CABI pp. 99-114.
35. Furgani G, Boszormenyi E, Fodor A, Mathe-Fodor A, Forst S, et al.(2008) Xenorhabdus antibiotics: a comparative analysis and potential utility for controlling mastitis caused by bacteria. J Appl Microbiol 104: 745-758.
36. Ji D, Kim Y, (2004) An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits the expression of an antibacterial peptide, cecropin, of the beet armyworm, Spodoptera exigua. J Insect Physiol 50: 489-496.
37. Akhurst RJ, Boemare N, (1990) Biology and taxonomy of Xenorhabdus. In: Gaugler R, Kaya HK, editors. Entomopathogenic nematodes in biological control Boca Raton CRC Press, Inc pp. 75-87.
38. Cowles KN, Cowles CE, Richards GR, Martens EC, Goodrich-Blair H, (2007) The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell Microbiol 9: 1311-1323.
39. Herbert EE, Cowles KN, Goodrich-Blair H, (2007) CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila. Appl Environ Microbiol 73: 7826-7836.
40. Park D, Forst S, (2006) Co-regulation of motility, exoenzyme and antibiotic production by the EnvZ-OmpR-FlhDC-FliA pathway in Xenorhabdus nematophila. Mol Microbiol 61: 1397-1412.
41. Richards GR, Goodrich-Blair H, (2010) Examination of Xenorhabdus nematophila lipases in pathogenic and mutualistic host interactions reveals a role for xlpA in nematode progeny production. Appl Environ Microbiol 76: 221-229.
42. Martens EC, Heungens K, Goodrich-Blair H, (2003) Early colonization events in the mutualistic association between Steinernema carpocapsae nematodes and Xenorhabdus nematophila bacteria. J Bacteriol 185: 3147-3154.
43. Popiel I, Grove DL, Friedman MJ, (1989) Infective juvenile formation in the insect parasitic nematode Steinernema feltiae. Parasitol 99: 77-81.
44. Herbert EE, Goodrich-Blair H, (2007) Friend and foe: the two faces of Xenorhabdus nematophila. Nat Rev Microbiol 5: 634-646.
45. Waterfield N, Bowen DJ, Fetherston JD, Perry RD, ffrench-Constant RH, (2001) The toxin complex genes of Photorhabdus: a growing gene family. Trends Microbiol 9: 185-191.
46. Clarke DJ, (2008) Photorhabdus: a model for the analysis of pathogenicity and mutualism. Cell Microbiol 10: 2159-2167.
47. Bennett HPJ, Clarke DJ, (2005) The pbgPE operon in Photorhabdus luminescens is required for pathogenicity and symbiosis. J Bacteriol 187: 77-84.
48. Derzelle S, Turlin E, Duchaud S, Pages S, Kunst F, et al.(2004) The PhoP-PhoQ two component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J Bacteriol 186: 1270-1279.
49. Eleftherianos I, Millichap PJ, ffrench-Constant RH, Reynolds SE, (2006) RNAi suppression of recognition protein mediated immune responses in the tobacco hornworm Manduca sexta causes increased susceptibility to the insect pathogen Photorhabdus. Devel Comp Immunol 30: 1099-1107.
50. Ji D, Kim Y, (2004) An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits the expression of an antibacterial peptide, cecropin, of the beet armyworm, Spodoptera exigua. J Insect Physiol 50: 489-496.
51. Park Y, Herbert EE, Cowles KN, Cowles CE, Menard ML, et al.(2007) Clonal variation in Xenorhabdus nematophila virulence and suppression of Manduca sexta immunity. Cell Microbiol 9: 645-656.
52. Easom CA, Joyce SA, Clarke DJ, (2010) Identification of genes involved in the mutualistic colonization of the nematode Heterorhabditis bacteriophora by the bacterium Photorhabdus luminescens. BMC Microbiol 10: 45.
53. Goodrich-Blair H, (2007) They've got a ticket to ride: Xenorhabdus nematophila-Steinernema carpocapsae symbiosis. Curr Opin Microbiol 10: 225-230.
54. Somvanshi VS, Kaufmann-Daszczuk B, Kim KS, Mallon S, Ciche TA, (2010) Photorhabdus phase variants express a novel fimbrial locus, mad, essential for symbiosis. Mol Microbiol 77: 1021-1038.
55. Ciche TA, Kim KS, Kaufmann-Daszczuk B, Nguyen KC, Hall DH, (2008) Cell invasion and matricide during Photorhabdus luminescens transmission by Heterorhabditis bacteriophora nematodes. Appl Environ Microbiol 74: 2275-2287.
56. Latreille P, Norton S, Goldman BS, Henkhaus J, Miller N, et al.(2007) Optical mapping as a routine tool in bacterial genome sequencing. BMC Genomics 8: 321.
57. Spiridonov SE, Krasomil-Osterfeld K, Moens M, (2004) Steinernema jollieti sp. n. (Rhabditida: Steinernematidae), a new entomopathogenic nematode from the American Midwest. Russ J Nematol 12: 85-95.
58. Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Givaudan A, et al.(2003) The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol 21: 1307-1313.
59. Wilkinson P, Waterfield NR, Crossman L, Corton C, Sanchez-Contreras M, et al.(2009) Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics 10: 302.
60. Ogier JC, Calteau A, Forst S, Goodrich-Blair H, Roche D, et al.(2010) Units of plasticity in bacterial genomes: new insight from the comparative genomics of two bacteria interacting with invertebrates, Photorhabdus and Xenorhabdus. BMC Genomics 11: 568.
61. Adams BJ, Fodor A, Koppenhöfer HS, Stackebrandt E, Stock SP, et al.(2006) Biodiversity and systematics of nematode-bacterium entomopathogens. Biol Control 37: 32-49.
62. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al.(1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392: 71.
63. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, et al.(2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57: 81-91.
64. Teeling H, Meyerdierks A, Bauer M, Amann R, Glockner FO, (2004) Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ Microbiol 6: 938-947.
65. Eisen JA, Heidelberg JF, White O, Salzberg SL, (2000) Evidence for symmetric chromosomal inversions around the replication origin in bacteria. Genome Biol 1: Research0011.
66. Suyama M, Bork P, (2001) Evolution of prokaryotic gene order: genome rearrangements in closely related species. Trends Genet 17: 10-13.
67. Srinivasan BS, Caberoy NB, Suen G, Taylor RG, Shah R, et al.(2005) Functional genome annotation through phylogenomic mapping. Nat Biotechnol 23: 691-698.
68. Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, et al.(2004) The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32: D258-261.
69. Brugirard-Ricaud K, Duchaud E, Givaudan A, Girard PA, Kunst F, et al.(2005) Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cell Microbiol 7: 363-371.
70. Blackburn M, Golubeva E, Bowen D, ffrench-Constant RH, (1998) A novel insecticidal toxin from Photorhabdus luminescens, toxin complex a (Tca), and its histopathological effects on the midgut of Manduca sexta. Appl Environ Microbiol 64: 3036-3041.
71. ffrench-Constant R, Waterfield N, (2006) An ABC guide to the bacterial toxin complexes. Adv Appl Microbiol 58: 169-183.
72. Brillard J, Ribeiro C, Boemare N, Brehelin M, Givaudan A, (2001) Two distinct hemolytic activities in Xenorhabdus nematophila are active against immunocompetent insect cells. Appl Environ Microbiol 67: 2515-2525.
73. Lanois A, Jubelin G, Givaudan A, (2008) FliZ, a flagellar regulator, is at the crossroads between motility, haemolysin expression and virulence in the insect pathogenic bacterium Xenorhabdus. Mol Microbiol 68: 516-533.
74. Brillard J, Duchaud E, Boemare N, Kunst F, Givaudan A, (2002) The PhlA hemolysin from the entomopathogenic bacterium Photorhabdus luminescens belongs to the two-partner secretion family of hemolysins. J Bacteriol 184: 3871-3878.
75. Aquilini E, Azevedo J, Jimenez N, Bouamama L, Tomas JM, et al.(2010) Functional identification of the Proteus mirabilis core lipopolysaccharide biosynthesis genes. J Bacteriol 192: 4413-4424.
76. An R, Sreevatsan S, Grewal PS, (2009) Comparative in vivo gene expression of the closely related bacteria Photorhabdus temperata and Xenorhabdus koppenhoeferi upon infection of the same insect host, Rhizotrogus majalis. BMC Genomics 10: 433.
77. Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, et al.(2004) Microbial factor-mediated development in a host-bacterial mutualism. Science 306: 1186-1188.
78. Ulevitch RJ, Tobias PS, (1995) Receptor-dependent mechanisms of cell stimulation by bacterial endotoxin. Annu Rev Immunol 13: 437-457.
79. Giannoulis P, Brooks CL, Dunphy GB, Mandato CA, Niven DF, et al.(2007) Interaction of the bacteria Xenorhabdus nematophila (Enterobactericeae) and Bacillus subtilis (Bacillaceae) with the hemocytes of larval Malacosoma disstria (Insecta: Lepidoptera: Lasiocampidae). J Invertebr Pathol 94: 20-30.
80. Mukherjee K, Altincicek B, Hain T, Domann E, Vilcinskas A, et al.(2010) Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol 76: 310-317.
81. Ardissone S, Kobayashi H, Kambara K, Rummel C, Noel KD, et al.(2011) Role of BacA in lipopolysaccharide synthesis, peptide transport, and nodulation by Rhizobium sp. strain NGR234. J Bacteriol 193: 2218-2228.
82. Ohta M, Watanabe A, Mikami T, Nakajima Y, Kitami M, et al.(2006) Mechanism by which Bombyx mori hemocytes recognize microorganisms: direct and indirect recognition systems for PAMPs. Dev Comp Immunol 30: 867-877.
83. Park D, Ciezki K, van der Hoeven R, Singh S, Reimer D, et al.(2009) Genetic analysis of xenocoumacin antibiotic production in the mutualistic bacterium Xenorhabdus nematophila. Mol Microbiol 73: 938-949.
84. Tan L, Grewal PS, (2001) Pathogenicity of Moraxella osloensis, a bacterium associated with the nematode Phasmarhabditis hermaphrodita, to the slug Deroceras reticulatum. Appl Environ Microbiol 67: 5010-5016.
85. Wu L, Holbrook C, Zaborina O, Ploplys E, Rocha F, et al.(2003) Pseudomonas aeruginosa expresses a lethal virulence determinant, the PA-I lectin/adhesin, in the intestinal tract of a stressed host: the role of epithelia cell contact and molecules of the Quorum Sensing Signaling System. Ann Surg 238: 754-764.
86. Kirkeby S, Hansen AK, d'Apice A, Moe D, (2006) The galactophilic lectin (PA-IL, gene LecA) from Pseudomonas aeruginosa. Its binding requirements and the localization of lectin receptors in various mouse tissues. Microb Pathog 40: 191-197.
87. Rebiere-Huet J, Di Martino P, Hulen C, (2004) Inhibition of Pseudomonas aeruginosa adhesion to fibronectin by PA-IL and monosaccharides: involvement of a lectin-like process. Can J Microbiol 50: 303-312.
88. Yoshida H, Fuwa TJ, Arima M, Hamamoto H, Sasaki N, et al.(2008) Identification of the Drosophila core 1 beta1,3-galactosyltransferase gene that synthesizes T antigen in the embryonic central nervous system and hemocytes. Glycobiol 18: 1094-1104.
89. Brugirard-Ricaud K, Givaudan A, Parkhill J, Boemare N, Kunst F, et al.(2004) Variation in the effectors of the type III secretion system among Photorhabdus species as revealed by genomic analysis. J Bacteriol 2004 4376-4381 pp. 4376-4381.
90. Gendlina I, Held KG, Bartra SS, Gallis BM, Doneanu CE, et al.(2007) Identification and type III-dependent secretion of the Yersinia pestis insecticidal-like proteins. Mol Microbiol 64: 1214-1227.
91. Richards GR, Herbert EE, Park Y, Goodrich-Blair H, (2008) Xenorhabdus nematophila lrhA is necessary for motility, lipase activity, toxin expression, and virulence in Manduca sexta insects. J Bacteriol 190: 4870-4879.
92. Khandelwal P, Banerjee-Bhatnagar N, (2003) Insecticidal activity associated with outer membrane vesicles of Xenorhabdus nematophilus. Appl Environ Microbiol 69: 2032-2037.
93. Bogdan C, Rollinghoff M, Diefenbach A, (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12: 64-76.
94. Eleftherianos I, Boundy S, Joyce SA, Aslam S, Marshall JW, et al.(2007) An antibiotic produced by an insect-pathogenic bacterium suppresses host defenses through phenoloxidase inhibition. Proc Natl Acad Sci U S A 104: 2419-2424.
95. Weiske J, Wiesner A, (1999) Stimulation of NO synthase activity in the immune-competent lepidopteran Estigmene acraea hemocyte line. Nitric Oxide 3: 123-131.
96. Chalabaev S, Turlin E, Charles JF, Namane A, Pages S, et al.(2007) The HcaR regulatory protein of Photorhabdus luminescens affects the production of proteins involved in oxidative stress and toxemia. Proteomics 7: 4499-4510.
97. Vivas EI, Goodrich-Blair H, (2001) Xenorhabdus nematophilus as a model for host-bacterium interactions: rpoS is necessary for mutualism with nematodes. J Bacteriol 183: 4687-4693.
98. An R, Grewal PS, (2010) Molecular mechanisms of persistence of mutualistic bacteria Photorhabdus in the entomopathogenic nematode host. PLoS One 5: e13154.
99. Watson RJ, Millichap P, Joyce SA, Reynolds S, Clarke DJ, (2010) The role of iron uptake in pathogenicity and symbiosis in Photorhabdus luminescens TT01. BMC Microbiol 10: 177.
100. Chasteen TG, Fuentes DE, Tantalean JC, Vasquez CC, (2009) Tellurite: history, oxidative stress, and molecular mechanisms of resistance. FEMS Microbiol Rev 33: 820-832.
101. Lyzen R, Wegrzyn G, (2005) Sensitivity of dark mutants of various strains of luminescent bacteria to reactive oxygen species. Arch Microbiol 183: 203-208.
102. Szpilewska H, Czyz A, Wegrzyn G, (2003) Experimental evidence for the physiological role of bacterial luciferase in the protection of cells against oxidative stress. Curr Microbiol 47: 379-382.
103. Bode HB, (2009) Entomopathogenic bacteria as a source of secondary metabolites. Curr Opin Chem Biol 13: 224-230.
104. Reimer D, Luxenburger E, Brachmann AO, Bode HB, (2009) A new type of pyrrolidine biosynthesis is involved in the late steps of xenocoumacin production in Xenorhabdus nematophila. Chembiochem 10: 1997-2001.
105. Joyce SA, Brachmann AO, Glazer I, Lango L, Schwar G, et al.(2008) Bacterial biosynthesis of a multipotent stilbene. Angew Chem Int Ed Engl 47: 1942-1945.
106. Sharma S, Waterfield N, Bowen D, Rocheleau T, Holland L, et al.(2002) The lumicins: novel bacteriocins from Photorhabdus luminescens with similarity to the uropathogenic-specific protein (USP) from uropathogenic Escherichia coli. FEMS Microbiol Lett 214: 241-249.
107. Fodor A, Fodor AM, Forst S, Hogan JS, Klein MG, et al.(2010) Comparative analysis of antibacterial activities of Xenorhabdus species on related and non-related bacteria in vivo. J Microbiol Antimicrob 2: 36-46.
108. Morales-Soto N, Forst SA, (2011) The xnp1 P2-like tail synthesis gene cluster encodes Xenorhabdicin and is required for interspecies competition. J Bacteriol 193: 3624-3632.
109. Singh J, Banerjee N, (2008) Transcriptional analysis and functional characterization of a gene pair encoding iron-regulated xenocin and immunity proteins of Xenorhabdus nematophila. J Bacteriol 190: 3877-3885.
110. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP, (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323: 741-746.
111. Gribaldo S, Brochier C, (2009) Phylogeny of prokaryotes: does it exist and why should we care? Res Microbiol 160: 513-521.
112. Cohan FM, (2002) What are bacterial species? Annu Rev Microbiol 56: 457-487.
113. Koeppel A, Perry EB, Sikorski J, Krizanc D, Warner A, et al.(2008) Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proc Natl Acad Sci U S A 105: 2504-2509.
114. Cohan FM, Perry EB, (2007) A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17: R373-386.
115. Ewing B, Green P, (1998) Base-calling of automated sequencer traces using Phred. II. error probabilities. Genome Res 8: 186-194.
116. Ewing B, Hillier L, Wendl MC, Green P, (1998) Base-calling of automated sequencer traces using Phred. I. accuracy assessment. Genome Res 8: 175-185.
117. Gordon D, Abajian C, Green P, (1998) Consed: a graphical tool for sequence finishing. Genome Res 8: 195-202.
118. Latreille P, Norton S, Goldman BS, Henkhaus J, Miller N, et al.(2007) Optical mapping as a routine tool for bacterial genome sequence finishing. BMC Genomics 8: 321.
119. Vallenet D, Labarre L, Rouy Z, Barbe V, Bocs S, et al.(2006) MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res 34: 53-65.
120. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
121. Felenstein J, (1989) PHYLIP- Phylogeny inference package (Version 3.2). Cladistocs 5.
122. Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, et al.(1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392: 71-75.
123. Vallenet D, Engelen S, Mornico D, Cruveiller S, Fleury L, et al.(2009) MicroScope: a platform for microbial genome annotation and comparative genomics. Database (Oxford) 2009 bap021 bap021.
124. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, et al.(2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12.
125. Richter M, Rossello-Mora R, (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106: 19126-19131.
126. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al.(1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
127. Davidson GS, Wylie BN, Boyack K, (2001) Cluster stability and the use of noise in interpretation of clustering. Proc IEEE Symp Inf Vis 2001 23-30 pp. 23-30.
128. Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, et al.(2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37: D211-215.