Elucidation of the Photorhabdus temperata genome and generation of a transposon mutant library to identify motility mutants altered in pathogenesis

Journal of Bacteriology

Volumn 197, Issue 13, 2015, Pages 2201-2216

  Hurst, Sheldon ^a   Rowedder, Holli ^a,b   Michaels, Brandye ^a,c   Bullock, Hannah ^a,d   Jackobeck, Ryan ^a,c   Abebe Akele, Feseha ^a   Durakovic, Umjia ^a   Gately, Jon ^a   Janicki, Erik ^a   Tisa, Louis S ^a  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b BOSTON COLLEGE   (United States)

^c Pfizer Biotech   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; POTASSIUM CHLORIDE; RNA; SODIUM CHLORIDE; BACTERIAL DNA; TRANSPOSON;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CONTROLLED STUDY; ENTOMOPATHOGENIC NEMATODE; EXTRACELLULAR SPACE; GENE IDENTIFICATION; GENE INSERTION; GENETIC COMPLEMENTATION; GENOME SIZE; HETERORHABDITIS BACTERIOPHORA; HOST PATHOGEN INTERACTION; MOLECULAR LIBRARY; NONHUMAN; PATHOGENESIS; PHOTORHABDUS; PHOTORHABDUS TEMPERATA; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; RNASE II GENE; SURFACE PROPERTY; SYMBIOSIS; TRANSPOSON; TWITCHING MOTILITY; WILD TYPE; ANIMAL; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; HOST PARASITE INTERACTION; MICROBIOLOGY; MOTH; MOVEMENT (PHYSIOLOGY); MUTATION; NEMATODE; PARASITOLOGY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); HETERORHABDITIS; HETERORHABDITIS BACTERIOPHORA; HEXAPODA; PHOTORHABDUS; PHOTORHABDUS TEMPERATA;

ANIMALS; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENE LIBRARY; GENOME, BACTERIAL; HOST-PARASITE INTERACTIONS; MOTHS; MOVEMENT; MUTATION; NEMATODA; PHOTORHABDUS; SYMBIOSIS;

EID: 84930795978     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00197-15     Document Type: Article

References (82)

1. Boemare N, Givaudan A, Brehelin M, Laumond C. 1997. Symbiosis and pathogenicity of nematode-bacterium complexes. Symbiosis 22:21-45.
2. Forst S, Dowds B, Boemare N, Stackebrandt E. 1997. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51:47-72. http://dx.doi.org/10.1146/annurev.micro.51.1.47.
3. Forst S, Nealson K. 1996. Molecular biology of the symbiotic pathogenic bacteria Xenorhabdus spp and Photorhabdus spp. Microbiol Rev 60:21-43.
4. Goodrich-Blair H, Clarke DJ. 2007. Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol Microbiol 64:260-268. http://dx.doi.org/10.1111/j.1365-2958.2007.05671.x.
5. Clarke DJ. 2008. Photorhabdus: a model for the analysis of pathogenicity and mutualism. Cell Microbiol 10:2159-2167. http://dx.doi.org/10.1111/j.1462-5822.2008.01209.x.
6. Waterfield NR, Ciche T, Clarke D. 2009. Photorhabdus and a host of hosts. Annu Rev Microbiol 63:557-574. http://dx.doi.org/10.1146/annurev.micro.091208.073507.
7. Burnell AM, Stock SP. 2000. Heterorhabditis, Steinernema and their bacterial symbionts-lethal pathogens of insects. Nematology 2:31-42. http://dx.doi.org/10.1163/156854100508872.
8. Fischer-Le Saux M, Viallard V, Brunel B, Normand P, Boemare NE. 1999. 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 49:1645-1656. http://dx.doi.org/10.1099/00207713-49-4-1645.
9. Boemare N. 2002. Interactions between the partners of the entomopathogenic bacterium nematode complexes, Steinernema-Xenorhabdus and Heterorhabditis-Photorhabdus. Nematology 4:601-603. http://dx.doi.org/10.1163/15685410260438863.
10. Ciche TA, Ensign JC. 2003. For the insect pathogen Photorhabdus luminescens, which end of a nematode is out? Appl Environ Microbiol 69:1890-1897. http://dx.doi.org/10.1128/AEM.69.4.1890-1897.2003.
11. Endo BY, Nickle WR. 1991. Ultrastructure of the intestinal epithelium, lumen, and associated bacteria in Heterorhabditis-Bacteriophora. J Helminthol Soc Wash 58:202-212.
12. Milstead JE. 1979. Heterorhabditis-Bacteriophora as a vector for introducing its associated bacterium into the hemocele of Galleria-Mellonella larvae. J Invertebr Pathol 33:324-327. http://dx.doi.org/10.1016/0022-2011(79)90033-8.
13. Poinar GOJ. 1975. Description and biology of a new insect parasite rhabditol, Heterorhabditis bactiophora n. gen, n sp (Rhabditida: Heterorhabditidae n fam). Nematologica 21:463-470. http://dx.doi.org/10.1163/187529275X00239.
14. Grewal PS, Koppenhofer AM, Choo HY. 2005. Lawn, turfgrass, and pasture applications, p 115-146. In Grewal PS, Ehlers R-U, Shapiro-Ilan DI (ed), Nematodes as biocontrol agents. CABI Publishing, Wallingford, United Kingdom,.
15. 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.
16. Bowen DJ, Ensign JC. 1998. Purification and characterization of a high-molecular-weight insecticidal protein complex produced by the entomopathogenic bacterium photorhabdus luminescens. Appl Environ Microbiol 64:3029-3035.
17. ffrench-Constant R, Bowen D. 1999. Photorhabdus toxins: novel biological insecticides. Curr Opin Microbiol 2:284-288. http://dx.doi.org/10.1016/S1369-5274(99)80049-6.
18. ffrench-Constant RH, Bowen DJ. 2000. Novel insecticidal toxins from nematode-symbiotic bacteria. Cell Mol Life Sci 57:828-833. http://dx.doi.org/10.1007/s000180050044.
19. Schmidt TM, Bleakley B, Nealson KH. 1988. Characterization of an extracellular protease from the insect pathogen Xenorhabdus luminescens. Appl Environ Microbiol 54:2793-2797.
20. Wang H, Dowds BC. 1993. Phase variation in Xenorhabdus luminescens: cloning and sequencing of the lipase gene and analysis of its expression in primary and secondary phases of the bacterium. J Bacteriol 175:1665-1673.
21. 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. http://dx.doi.org/10.1128/AEM.67.6.2515-2525.2001.
22. Thomas GM, Poinar GO. 1979. Xenorhabdus gen. nov., a genus of entomopathogenic, nematophilic bacteria of the family Enterobacteriaceae. Int J Syst Bacteriol 29:352-360. http://dx.doi.org/10.1099/00207713-29-4-352.
23. 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.
24. Richardson WH, Schmidt TM, Nealson KH. 1988. Identification of an anthraquinone pigment and a hydroxystilbene antibiotic from Xenorhabdus luminescens. Appl Environ Microbiol 54:1602-1605.
25. Derzelle S, Ngo S, Turlin E, Duchaud E, Namane A, Kunst F, Danchin A, Bertin P, Charles JF. 2004. AstR-AstS, a new two-component signal transduction system, mediates swarming, adaptation to stationary phase and phenotypic variation in Photorhabdus luminescens. Microbiology 150:897-910. http://dx.doi.org/10.1099/mic.0.26563-0.
26. Akhurst RJ. 1980. Morphological and functional dimorphism in Xenorhabdus spp bacteria symbiotically associated with the insect pathogenic nematodes Neoaplectana and Heterorhabditis. J Gen Microbiol 121:303-309.
27. Boemare N, Thaler JO, Lanois A. 1997. Simple bacteriological tests for phenotypic characterization of Xenorhabdus and Photorhabdus phase variants. Symbiosis 22:167-175.
28. Rosner BM, Ensign JC, Schink B. 1996. Anaerobic metabolism of primary and secondary forms of Photorhabdus luminescens. FEMS Microbiol Lett 140:227-232. http://dx.doi.org/10.1111/j.1574-6968.1996.tb08341.x.
29. Smigielski AJ, Akhurst RJ, Boemare NE. 1994. Phase variation in Xenorhabdus nematophilus and Photorhabdus luminescens-differences in respiratory activity and membrane energization. Appl Environ Microbiol 60:120-125.
30. Gaudriault S, Pages S, Lanois A, Laroui C, Teyssier C, Jumas-Bilak E, Givaudan A. 2008. Plastic architecture of bacterial genome revealed by comparative genomics of Photorhabdus variants. Genome Biol 9:R117. http://dx.doi.org/10.1186/gb-2008-9-7-r117.
31. Hodgson MM, Day B, White DJ, Tisa LS. 2003. Effect of growth conditions on the motility of Photorhabdus temperata. Arch Microbiol 180:17-24. http://dx.doi.org/10.1007/s00203-003-0558-z.
32. Michaels B, Tisa LS. 2011. Swarming motility by Photorhabdus temperata is influenced by environmental conditions and uses the same flagella as that used in swimming motility. Can J Microbiol 57:196-203. http://dx.doi.org/10.1139/W10-119.
33. Ehlers R-U, Stoessel S, Wyss U. 1990. The influence of phase variants of Xenorhabdus spp. and Escherichia coli (Enterobacteriaceae) on the propagation of entomopathogenic nematodes of the genera Steinernema and Heterorhabditis. Rev Nematol 13:417-424.
34. Han RC, Ehlers RU. 2001. Effect of Photorhabdus luminescens phase variants on the in vivo and in vitro development and reproduction of the entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae. FEMS Microbiol Ecol 35:239-247. http://dx.doi.org/10.1111/j.1574-6941.2001.tb00809.x.
35. Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Givaudan A, Taourit S, Bocs S, Boursaux-Eude C, Chandler M, Charles JF, Dassa E, Derose R, Derzelle S, Freyssinet G, Gaudriault S, Medigue C, Lanois A, Powell K, Siguier P, Vincent R, Wingate V, Zouine M, Glaser P, Boemare N, Danchin A, Kunst F. 2003. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol 21:1307-1313. http://dx.doi.org/10.1038/nbt886.
36. Wilkinson P, Waterfield NR, Crossman L, Corton C, Sanchez-Contreras M, Vlisidou I, Barron A, Bignell A, Clark L, Ormond D, Mayho M, Bason N, Smith F, Simmonds M, Churcher C, Harris D, Thompson NR, Quail M, Parkhill J, Ffrench-Constant RH. 2009. Comparative genomics of the emerging human pathogen Photorhabdus asymbiotica with the insect pathogen Photorhabdus luminescens. BMC Genomics 10:302. http://dx.doi.org/10.1186/1471-2164-10-302.
37. ffrench-Constant R, Waterfield Daborn N, Joyce P, Bennett S, Au H, Dowling C, Boundy A, Reynolds S, Clarke SD. 2003. Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev 26:433-456. http://dx.doi.org/10.1111/j.1574-6976.2003.tb00625.x.
38. Easom CA, Clarke DJ. 2008. Motility is required for the competitive fitness of entomopathogenic Photorhabdus luminescens during insect infection. BMC Microbiol 8:168. http://dx.doi.org/10.1186/1471-2180-8-168.
39. Boemare NE, Akhurst RJ, Mourant RG. 1993. DNA relatedness between Xenorhabdus spp (Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes, and a proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen nov. Int J Syst Bacteriol 43:249-255. http://dx.doi.org/10.1099/00207713-43-2-249.
40. Poinar GOJ, Jackson T, Klein M. 1987. Heterorhabdus megidis sp. n. (Heterorhabditidae: Rhabdittida), parasitic on Japanese beetle, Popilla japonica (Scaraarabaeidedae: Coleoptera) in Ohio. Proc Helminthol Soc Wash 54:53-59.
41. Darling AE, Mau B, Perna NT. 2010. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147. http://dx.doi.org/10.1371/journal.pone.0011147.
42. Markowitz VM, Korzeniewski F, Palaniappan K, Szeto E, Werner G, Padki A, Zhao XL, Dubchak I, Hugenholtz P, Anderson I, Lykidis A, Mavromatis K, Ivanova N, Kyrpides NC. 2006. The integrated microbial genomes (IMG) system. Nucleic Acids Res 34:D344-D348. http://dx.doi.org/10.1093/nar/gkj024.
43. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMCBioinformatics 11:119. http://dx.doi.org/10.1186/1471-2105-11-119.
44. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955-964. http://dx.doi.org/10.1093/nar/25.5.0955.
45. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glockner FO. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188-7196. http://dx.doi.org/10.1093/nar/gkm864.
46. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882. http://dx.doi.org/10.1093/nar/25.24.4876.
47. Lerat E, Daubin V, Ochman H, Moran NA. 2005. Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3:807-814. http://dx.doi.org/10.1371/journal.pbio.0030130.
48. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likeli-hood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
49. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis comparison tool. Bioinformatics 21:3422-3423. http://dx.doi.org/10.1093/bioinformatics/bti553.
50. Blin K, Medema MH, Kazempour D, Fischbach MA, Breitling R, Takano E, Weber T. 2013. antiSMASH 2.0 -a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res 41: W204-W212. http://dx.doi.org/10.1093/nar/gkt449.
51. Medema MH, Blin K, Cimermancic P, de Jager V, Zakrzewski P, Fischbach MA, Weber T, Takano E, Breitling R. 2011. antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences. Nucleic Acids Res 39:W339-W346. http://dx.doi.org/10.1093/nar/gkr466.
52. Ciche TA, Bintrim SB, Horswill AR, Ensign JC. 2001. A Phosphopantetheinyl transferase homolog is essential for Photorhabdus luminescens to support growth and reproduction of the entomopathogenic nematode Heterorhabditis bacteriophora. J Bacteriol 183:3117-3126. http://dx.doi.org/10.1128/JB.183.10.3117-3126.2001.
53. Chan JWYF, Goodwin PH. 1994. Extraction of genomic DNA from extracellular polysaccharide-synthesizing Gram-negative bacteria. Biotechniques 18:419-422.
54. Rawnsley T, Tisa LS. 2007. Development of a physical map for three Frankia strains and a partial genetic map for Frankia EuI1c. Physiol Plantarum 130:427-439. http://dx.doi.org/10.1111/j.1399-3054.2007.00896.x.
55. Han RC, Ehlers RU. 2000. Pathogenicity, development, and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. J Invertebr Pathol 75:55-58. http://dx.doi.org/10.1006/jipa.1999.4900.
56. Clarke DJ, Dowds BCA. 1995. Virulence mechanisms of Photorhabdus sp strain K122 toward wax moth larvae. J Invertebr Pathol 66:149-155. http://dx.doi.org/10.1006/jipa.1995.1078.
57. Bilgrami AL, Gaugler R, Shapiro-Ilan DI, Adams BJ. 2006. Source of trait deterioration in entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae during in vivo culture. Nematology 8:397-409. http://dx.doi.org/10.1163/156854106778493394.
58. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121-4130.
59. Tailliez P, Pages S, Edgington S, Tymo LM, Buddie AG. 2012. Description of Xenorhabdus magdalenensis sp. nov., the symbiotic bacterium associated with Steinernema australe. Int J Syst Evol Microbiol 62:1761-1765. http://dx.doi.org/10.1099/ijs.0.034322-0.
60. Tailliez P, Laroui C, Ginibre N, Paule A, Pages S, Boemare N. 2010. Phylogeny of Photorhabdus and Xenorhabdus based on universally conserved protein-coding sequences and implications for the taxonomy of these two genera. Proposal of new taxa: X. vietnamensis sp. nov., P. luminescens subsp. caribbeanensis subsp. nov., P. luminescens subsp. hainanensis subsp. nov., P. temperata subsp. khanii subsp. nov., P. temperata subsp. tasmaniensis subsp. nov., and the reclassification of P. luminescens subsp. thracensis as P. temperata subsp. thracensis comb. nov. Int J Syst Evol Microbiol 60:1921-1937. http://dx.doi.org/10.1099/ijs.0.014308-0.
61. Ciche TA, Blackburn M, Carney JR, Ensign JC. 2003. Photobactin: a catechol siderophore produced by Photorhabdus luminescens, an entomopathogen mutually associated with Heterorhabditis bacteriophora NC1 nematodes. Appl Environ Microbiol 69:4706-4713. http://dx.doi.org/10.1128/AEM.69.8.4706-4713.2003.
62. Brachmann AO, Joyce SA, Jenke-Kodama H, Schwar G, Clarke DJ, Bode HB. 2007. A type II polyketide synthase is responsible for anthraquinone biosynthesis in Photorhabdus luminescens. Chembiochem 8:1721-1728. http://dx.doi.org/10.1002/cbic.200700300.
63. Joyce SA, Lango L, Clarke DJ. 2011. The regulation of secondary metabolism and mutualism in the insect pathogenic bacterium Photorhabdus luminescens. Adv Appl Microbiol 76:1-25. http://dx.doi.org/10.1016/B978-0-12-387048-3.00001-5.
64. Li JX, Chen GH, Wu HM, Webster JM. 1995. Identification of two pigments and a hydroxystilbene antibiotic from Photorhabdus luminescens. Appl Environ Microbiol 61:4329-4333.
65. Bode HB, Reimer D, Fuchs SW, Kirchner F, Dauth C, Kegler C, Lorenzen W, Brachmann AO, Grun P. 2012. Determination of the absolute configuration of peptide natural products by using stable isotope labeling and mass spectrometry. Chemistry 18:2342-2348. http://dx.doi.org/10.1002/chem.201103479.
66. Brachmann AO, Brameyer S, Kresovic D, Hitkova I, Kopp Y, Manske C, Schubert K, Bode HB, Heermann R. 2013. Pyrones as bacterial signaling molecules. Nat Chem Biol 9:573-578. http://dx.doi.org/10.1038/nchembio.1295.
67. Theodore CM, King JB, You JL, Cichewicz RH. 2012. Production of cytotoxic glidobactins/luminmycins by Photorhabdus asymbiotica in liquid media and live crickets. J Nat Prod 75:2007-2011. http://dx.doi.org/10.1021/np300623x.
68. Derzelle S, Duchaud E, Kunst F, Danchin A, Bertin P. 2002. Identification, characterization, and regulation of a cluster of genes involved in carbapenem biosynthesis in Photorhabdus luminescens. Appl Environ Microbiol 68:3780-3789. http://dx.doi.org/10.1128/AEM.68.8.3780-3789.2002.
69. Joyce SA, Brachmann AO, Glazer I, Lango L, Schwar G, Clarke DJ, Bode HB. 2008. Bacterial biosynthesis of a multipotent stilbene. Angew Chem Int Ed 47:1942-1945. http://dx.doi.org/10.1002/anie.200705148.
70. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. 2009. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10:104. http://dx.doi.org/10.1186/1471-2164-10-104.
71. Chaston JM, Suen G, Tucker SL, Andersen AW, Bhasin A, Bode E, Bode HB, Brachmann AO, Cowles CE, Cowles KN, Darby C, de Leon L, Drace K, Du Z, Givaudan A, Herbert Tran EE, Jewell KA, Knack JJ, Krasomil-Osterfeld KC, Kukor R, Lanois A, Latreille P, Leimgruber NK, Lipke CM, Liu R, Lu X, Martens EC, Marri PR, Medigue C, Menard ML, Miller NM, Morales-Soto N, Norton S, Ogier JC, Orchard SS, Park D, Park Y, Qurollo BA, Sugar DR, Richards GR, Rouy Z, Slominski B, Slominski K, Snyder H, Tjaden BC, van der Hoeven R, Welch RD, Wheeler C, Xiang B, Barbazuk B, Gaudriault S, Goodner B, Slater SC, Forst S, Goldman BS, Goodrich-Blair H. 2011. The entomopathogenic bacterial endosymbionts Xenorhabdus and Photorhabdus: convergent lifestyles from divergent genomes. PLoS One 6:e27909. http://dx.doi.org/10.1371/journal.pone.0027909.
72. Shrivastava S, Mande SS. 2008. Identification and functional characterization of gene components of type VI secretion system in bacterial genomes. PLoS One 3:e2955. http://dx.doi.org/10.1371/journal.pone.0002955.
73. Chow J, Mazmanian SK. 2010. A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 7:265-276. http://dx.doi.org/10.1016/j.chom.2010.03.004.
74. Waterfield NR, Daborn PJ, ffrench-Constant, RH. 2002. Genomic islands in Photorhabdus. Trends Microbiol 10:541-545. http://dx.doi.org/10.1016/S0966-842X(02)02463-0.
75. Brugirard-Ricaud K, Givaudan A, Parkhill J, Boemare N, Kunst F, Zumbihl R, Duchaud E. 2004. Variation in the effectors of the type III secretion system among Photorhabdus species as revealed by genomic analysis. J Bacteriol 186:4376-4381. http://dx.doi.org/10.1128/JB.186.13.4376-4381.2004.
76. Brugirard-Ricaud K, Duchaud E, Givaudan A, Girard PA, Kunst F, Boemare N, Brehelin M, Zumbihl R. 2005. Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cell Microbiol 7:363-371. http://dx.doi.org/10.1111/j.1462-5822.2004.00466.x.
77. Frazao C, Mcvey CE, Amblar M, Barbas A, Vonrhein C, Arraiano CM, Carrondo MA. 2006. Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443:110-114. http://dx.doi.org/10.1038/nature05080.
78. Lu F, Taghbalout A. 2014. The Escherichia coli major exoribonuclease RNase II is a component of the RNA degradosome. Biosci Rep 34:e00166. http://dx.doi.org/10.1042/BSR20140113.
79. Tsao MY, Lin TL, Hsieh PF, Wang JT. 2009. The 3'-to-5' exoribonuclease (encoded by HP1248) of Helicobacter pylori regulates motility and apoptosis-inducing genes. J Bacteriol 191:2691-2702. http://dx.doi.org/10.1128/JB.01182-08.
80. Matos RG, Barria C, Moreira RN, Barahona S, Domingues S, Arraiano CM. 2014. The importance of proteins of the RNase II/RNB-family in pathogenic bacteria. Front Cell Infect Microbiol 4:68. http://dx.doi.org/10.3389/fcimb.2014.00068.
81. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. http://dx.doi.org/10.1093/bioinformatics/btm404.
82. Felsenstein J. 1985. Confidence limits on phylogenies-an approach using the bootstrap. Evolution 39:783-791. http://dx.doi.org/10.2307/2408678.