Transcriptional analysis of a photorhabdus sp. variant reveals transcriptional control of phenotypic variation and multifactorial pathogenicity in insects

Applied and Environmental Microbiology

Volumn 77, Issue 3, 2011, Pages 1009-1020

  Lanois, A ^a   Pages, S ^a   Bourot, S ^b   Canoy, A S ^c   Givaudan, A ^a   Gaudriault, S ^a  

^a UNIV MONTPELLIER   (France)

^b Bayer sa nv Belgium   (Belgium)

^c UNIVERSITÉ DE HAUTE ALSACE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENTOMOPATHOGENIC NEMATODE; GENES ENCODING; LIPASE ACTIVITY; OVER-EXPRESSION; OXIDATIVE STRESS RESPONSE; PHENOTYPIC TRAITS; PHENOTYPIC VARIATIONS; TRANSCRIPTIONAL ANALYSIS; TRANSCRIPTIONAL CONTROL; WILD TYPES;

BACTERIOLOGY; BLOOD; GENES; METABOLITES; TRANSCRIPTION;

VALUE ENGINEERING;

BACTERIAL PROTEIN;

BACTERIUM; ENTOMOPATHOGENIC ORGANISM; ENZYME ACTIVITY; INSECTICIDE; MOTH; MUTUALISM; NEMATODE; PATHOGENICITY; PHENOTYPIC PLASTICITY; TOXICITY; VIRULENCE;

ANIMAL; ARMYWORM; ARTICLE; CLASSIFICATION; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHENOTYPE; PHOTORHABDUS; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC VARIATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PHOTORHABDUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPODOPTERA; VIRULENCE;

HEXAPODA; NEMATODA; PHOTORHABDUS; PHOTORHABDUS LUMINESCENS; PHOTORHABDUS SP.; SPODOPTERA LITTORALIS;

EID: 79551485762     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01696-10     Document Type: Article

References (69)

1. Akhurst, R. J. 1980. Morphological and functional dimorphism in Xenorh-abdus spp., bacteria symbiotically associated with the insect pathogenic nem-atodes Neoaplectana and Heterorhabditis. J. Gen. Microbiol. 121:303-309.
2. Ausubel, F. M., et al. 1993. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, NY.
3. Beier, D., and R. Gross. 2006. Regulation of bacterial virulence by two-component systems. Curr. Opin. Microbiol. 9:143-152.
4. Bintrim, S. B., and J. C. Ensign. 1998. Insertional inactivation of genes encoding the crystalline inclusion proteins of Photorhabdus luminescens results in mutants with pleiotropic phenotypes. J. Bacteriol. 180:1261-1269.
5. Boemare, N., J.-O. Thaler, and A. Lanois. 1997. Simple bacteriological tests for phenotypic characterization of Xenorhabdus and Photorhabdus phase variants. Symbiosis 22:167-175.
6. Boemare, N. E. 2002. Biology, taxonomy, and systematics of Photorhabdus and Xenorhabdus, p. 35-56. In R. Gaugler (ed.), Entomopathogenic nema-tology. CABI Publishing, Wallingford, United Kingdom.
7. Boemare, N. E., and R. J. Akhurst. 1988. Biochemical and physiological characterization of colony form variants in Xenorhabdus spp. (Enterobacte-riaceae). J. Gen. Microbiol. 134:751-761.
8. Bowen, D., et al. 1998. Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280:2129-2132.
9. Bowen, D. J., et al. 2003. Genetic and biochemical characterization of PrtA, an RTX-like metalloprotease from Photorhabdus. Microbiology 149:1581- 1591.
10. Brachmann, A. O., et al. 2007. A type II polyketide synthase is responsible for anthraquinone biosynthesis in Photorhabdus luminescens. Chembiochem 8:1721-1728.
11. Brillard, J., E. Duchaud, N. Boemare, F. Kunst, and A. Givaudan. 2002. The PhlA hemolysin from the entomopathogenic bacterium Photorhabdus lumi-nescens belongs to the two-partner secretion family of hemolysins. J. Bacte-riol. 184:3871-3878.
12. Brugirard-Ricaud, K., et al. 2005. Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cell Microbiol. 7:363-371.
13. Bunny, K. L., R. M. Hall, and H. W. Stokes. 1995. New mobile gene cassettes containing an aminoglycoside resistance gene, aacA7, and a chloramphenicol resistance gene, catB3, in an integron in pBWH301. Antimicrob. Agents Chemother. 39:686-693.
14. Cabral, C. M., A. Cherqui, A. Pereira, and N. Simoes. 2004. Purification and characterization of two distinct metalloproteases secreted by the ento-mopathogenic bacterium Photorhabdus sp. strain Az29. Appl. Environ. Mi-crobiol. 70:3831-3838.
15. Carfi, A., et al. 1995. The 3-D structure of a zinc metallo-beta- lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J. 14:4914- 4921.
16. Chalabaev, S., et al. 2008. Cinnamic acid, an autoinducer of its own biosynthesis, is processed via Hca enzymes in Photorhabdus luminescens. Appl. Environ. Microbiol. 74:1717-1725.
17. Chalabaev, 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.
18. Clarke, D. J. 2008. Photorhabdus: a model for the analysis of pathogenicity and mutualism. Cell Microbiol. 10:2159-2167.
19. Daborn, P. J., et al. 2002. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc. Natl. Acad. Sci. U. S. A. 99:10742-10747.
20. Dellagi, A., M. N. Brisset, J. P. Paulin, and D. Expert. 1998. Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Mol. Plant-Microbe Interact. 11:734-742.
21. Derzelle, S., E. Duchaud, F. Kunst, A. Danchin, and P. Bertin. 2002. Identification, characterization, and regulation of a cluster of genes involved in carbapenem biosynthesis in Photorhabdus luminescens. Appl. Environ. Mi-crobiol. 68:3780-3789.
22. Derzelle, S., et al. 2004. AstR-AstS, a new two-component signal transduc-tion system, mediates swarming, adaptation to stationary phase and pheno-typic variation in Photorhabdus luminescens. Microbiology 150:897-910.
23. Derzelle, S., et al. 2004. The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J. Bacteriol. 186:1270-1279.
24. Duchaud, E., et al. 2003. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat. Biotechnol. 21:1307-1313.
25. ffrench-Constant, R., et al. 2003. Photorhabdus: toward a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol. Rev. 26:433-456.
26. Fischer-Le Saux, M., V. Viallard, B. Brunel, P. Normand, and N. E. Bo-emare. 1999. Polyphasic classification of the genus Photorhabdus and proposal of new taxa: P. luminescens subsp. luminescens subsp. nov., P. lumine-scens 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 Pt. 4:1645-1656.
27. Forst, S., and D. Clarke. 2002. Bacteria-nematode symbiosis, p. 57-77. In R. Gaugler (ed.), Entomopathogenic nematology. CAB International, Walling-ford, Oxfordshire, United Kingdom.
28. Forst, S., B. Dowds, N. Boemare, and E. Stackebrandt. 1997. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51:47-72.
29. Frackman, S., M. Anhalt, and K. H. Nealson. 1990. Cloning, organization, and expression of the bioluminescence genes of Xenorhabdus luminescens. J. Bacteriol. 172:5767-5773.
30. Gaudriault, S., et al. 2006. Whole-genome comparison between Photorhab-dus strains to identify genomic regions involved in the specificity of nema-tode interaction. J. Bacteriol. 188:809-814.
31. Gaudriault, S., et al. 2008. Plastic architecture of bacterial genome revealed by comparative genomics of Photorhabdus variants. Genome Biol. 9:R117.
32. Gerritsen, L. J., G. de Raay, and P. H. Smits. 1992. Characterization of form variants of Xenorhabdus luminescens. Appl. Environ. Microbiol. 58:1975- 1979.
33. Givaudan, A., and A. Lanois. 2000. flhDC, the flagellar master operon of Xenorhabdus nematophilus: requirement for motility, lipolysis, extracellular hemolysis, and full virulence in insects. J. Bacteriol. 182:107-115.
34. Gunn, J. S., et al. 1998. PmrA-PmrB-regulated genes necessary for 4-ami-noarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27:1171-1182.
35. Gunn, J. S., S. S. Ryan, J. C. Van Velkinburgh, R. K. Ernst, and S. I. Miller. 2000. Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar Typhimurium. Infect. Im-mun. 68:6139-6146.
36. Hantke, K. 2001. Iron and metal regulation in bacteria. Curr. Opin. Micro-biol. 4:172-177.
37. Hay, N. A., D. J. Tipper, D. Gygi, and C. Hughes. 1999. A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabi-lis. J. Bacteriol. 181:2008-2016.
38. Hu, K., and J. M. Webster. 1998. In vitro and in vivo characterization of a small-colony variant of the primary form of Photorhabdus luminescens MD (Enterobacteriaceae). Appl. Environ. Microbiol. 64:3214-3219.
39. Hurlbert, R. E., J. Xu, and C. L. Small. 1989. Colonial and cellular polymorphism in Xenorhabdus luminescens. Appl. Environ. Microbiol. 55:1136- 1143.
40. Joyce, S. A., and D. J. Clarke. 2003. A hexA homologue from Photorhabdus regulates pathogenicity, symbiosis, and phenotypic variation. Mol. Microbiol. 47:1445-1457.
41. Joyce, S. A., R. J. Watson, and D. J. Clarke. 2006. The regulation of patho-genicity and mutualism in Photorhabdus. Curr. Opin. Microbiol. 9:127-132.
42. Kovach, M. E., et al. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 66:175-176.
43. Krin, E., et al. 2006. Pleiotropic role of quorum-sensing autoinducer 2 in Photorhabdus luminescens. Appl. Environ. Microbiol. 72:6439-6451.
44. Krin, E., et al. 2008. Regulatory role of UvrY in adaptation of Photorhabdus luminescens growth inside the insect. Environ. Microbiol. 10:1118-1134.
45. Kvint, K., L. Nachin, A. Diez, and T. Nyström. 2003. The bacterial universal stress protein: function and regulation. Curr. Opin. Microbiol. 6:140-145.
46. Lanois, A., G. Jubelin, and A. Givaudan. 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.
47. Li, M., et al. 2008. Expression and activity of a probable toxin from Pho-torhabdus luminescens. Mol. Biol. Rep. 36:785-790.
48. Lynch, A. S., and E. C. C. Lin. 1996. Responses to molecular oxygen, p. 1526-1535. In F. C. Neidhart et al. (ed.), Escherichia coli and Salmonella, vol. 1. ASM Press, Washington, DC.
49. Marokhazi, J., et al. 2004. Comparison of proteolytic activities produced by entomopathogenic Photorhabdus bacteria: strain- and phase-dependent heterogeneity in composition and activity of four enzymes. Appl. Environ. Microbiol. 70:7311-7320.
50. Moureaux, N., T. Karjalainen, A. Givaudan, P. Bourlioux, and N. Boemare. 1995. Biochemical characterization and agglutinating properties of Xenorh-abdus nematophilus F1 fimbriae. Appl. Environ. Microbiol. 61:2707-2712.
51. Nappi, A. J., and E. Ottaviani. 2000. Cytotoxicity and cytotoxic molecules in invertebrates. Bioessays 22:469-480.
52. Nappi, A. J., and E. Vass. 1998. Hydrogen peroxide production in immune-reactive Drosophila melanogaster. J. Parasitol. 84:1150-1157.
53. O'Neill, K. H., D. M. Roche, D. J. Clarke, and B. C. Dowds. 2002. The ner gene of Photorhabdus: effects on primary-form-specific phenotypes and outer membrane protein composition. J. Bacteriol. 184:3096-3105.
54. Ong, K. L., and F. N. Chang. 1997. Analysis of proteins from different phase variants of the entomopathogenic bacteria Photorhabdus luminescens by two-dimensional zymography. Electrophoresis 18:834-839.
55. Prilipov, A., P. S. Phale, R. Koebnik, C. Widmer, and J. P. Rosenbusch. 1998. Identification and characterization of two quiescent porin genes, nmpC and ompN, in Escherichia coli BE. J. Bacteriol. 180:3388-3392.
56. Sabri, M., S. Leveille, and C. M. Dozois. 2006. A SitABCD homologue from an avian pathogenic Escherichia coli strain mediates transport of iron and manganese and resistance to hydrogen peroxide. Microbiology 152:745-758.
57. Sandegren, L., and D. I. Andersson. 2009. Bacterial gene amplification: implications for the evolution of antibiotic resistance. Nat. Rev. Microbiol. 7:578-588.
58. Sharma, S., 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.
59. Sicard, M., et al. 2004. Stages of infection during the tripartite interaction between Xenorhabdus nematophila, its nematode vector, and insect hosts. Appl. Environ. Microbiol. 70:6473-6480.
60. Simon, R., U. Priefer, and A. Pülher. 1983. A broad hostrange mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology (NY) 1:784-791.
61. Turlin, E., et al. 2006. Proteome analysis of the phenotypic variation process in Photorhabdus luminescens. Proteomics 6:2705-2725.
62. Vollmer, W., M. von Rechenberg, and J. V. Holtje. 1999. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol. Chem. 274:6726-6734.
63. Wang, H., and B. C. Dowds. 1993. Phase variation in Xenorhabdus lumine-scens: 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.
64. Wang, H., and B. C. A. Dowds. 1991. Molecular cloning and characterization of the lux genes from the secondary form of Xenorhabdus luminescens K122. Biochem. Soc. Trans. 20:68S.
65. Wang, Y., A. L. Bilgrami, D. Shapiro-Ilan, and R. Gaugler. 2007. Stability of entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus lu-minescens, during in vitro culture. J. Ind. Microbiol. Biotechnol. 34:73-81.
66. Waterfield, N., S. G. Kamita, B. D. Hammock, and R. ffrench-Constant. 2005. The Photorhabdus Pir toxins are similar to a developmentally regulated insect protein but show no juvenile hormone esterase activity. FEMS Mi-crobiol. Lett. 245:47-52.
67. Waterfield, N. R., T. Ciche, and D. Clarke. 2009. Photorhabdus and a host of hosts. Annu. Rev. Microbiol. 63:557-574.
68. Williams, J. S., M. Thomas, and D. J. Clarke. 2005. The gene stlA encodes a phenylalanine ammonia-lyase that is involved in the production of a stil-bene antibiotic in Photorhabdus luminescens TT01. Microbiology 151:2543- 2550.
69. Wouts, W. M. 1990. The primary form of Xenorhabdus species (Enterobac-teriaceae, Eubacteriales) may consist of more than one bacterial species. Nematologica 36:313-318.