CpxRA regulates mutualism and pathogenesis in Xenorhabdus nematophila

Applied and Environmental Microbiology

Volumn 73, Issue 24, 2007, Pages 7826-7836

  Herbert, Erin E ^a   Cowles, Kimberly N ^a,b   Goodrich Blair, Heidi ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; ESCHERICHIA COLI; LIPASES; PATHOGENS;

CELL MORPHOLOGY; MUTUALISTIC INTERACTIONS; XENORHABDUS NEMATOPHILA;

SIGNAL TRANSDUCTION;

BETA GALACTOSIDASE; HEMOLYSIN; PILIN; PROTEINASE; TRIACYLGLYCEROL LIPASE;

BACTERIUM; ENTOMOPATHOGENIC ORGANISM; MORPHOLOGY; MOTILITY; MUTUALISM; PATHOGEN;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; CELL STRUCTURE; CONTROLLED STUDY; CPXRA GENE; ENTOMOPATHOGENY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC CODE; GENETIC TRANSCRIPTION; HEMOLYMPH; MANDUCA SEXTA; MOLECULAR INTERACTION; NEMATODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEINERNEMA CARPOCAPSAE; SYMBIOSIS; WILD TYPE; XENORHABDUS NEMATOPHILA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTI-BACTERIAL AGENTS; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; DNA, BACTERIAL; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GRAM-NEGATIVE BACTERIAL INFECTIONS; HEMOLYSIN PROTEINS; LIPASE; LOCOMOTION; MANDUCA; MOLECULAR SEQUENCE DATA; NEMATODA; PEPTIDE HYDROLASES; PROTEIN KINASES; SEQUENCE ANALYSIS, DNA; SURVIVAL ANALYSIS; XENORHABDUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HEXAPODA; MANDUCA SEXTA; NEMATODA; STEINERNEMA CARPOCAPSAE; XENORHABDUS NEMATOPHILA;

EID: 37349026222     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01586-07     Document Type: Article

References (79)

1. Akhurst, R. J. 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.
2. Bailey, T. L., and C. Elkan. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2:28-36.
3. Banerjee, J., J. Singh, M. C. Joshi, S. Ghosh, and N. Banerjee. 2006. The cytotoxic fimbrial structural subunit of Xenorhabdus nematophila is a pore-forming toxin. J. Bacteriol. 188:7957-7962.
4. Bao, Y., D. P. Lies, H. Fu, and G. P. Roberts. 1991. An improved Tn7-based system for the single-copy insertion of cloned genes into chromosomes of gram-negative bacteria. Gene 109:167-168.
5. Batchelor, E., D. Walthers, L. J. Kenney, and M. Goulian. 2005. The Escherichia coli CpxA-CpxR envelope stress response system regulates expression of the porins ompF and ompC. J. Bacteriol. 187:5723-5731.
6. Bird, A. F., and R. J. Akhurst. 1983. The nature of the intestinal vesicle in nematodes of the family Steinernematidae. Int. J. Parasitol. 13:599-606.
7. 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.
8. Brillard, J., C. Ribeiro, N. Boemare, M. Brehelin, and A. Givaudan. 2001. Two distinct hemolytic activities in Xenorhabdus nematophila are active against immunocompetent insect cells. Appl. Environ. Microbiol. 67:2515-2525.
9. Caldas, C., A. Cherqui, A. Pereira, and N. Simoes. 2002. Purification and characterization of an extracellular protease from Xenorhabdus nematophila involved in insect immunosuppression. Appl. Environ. Microbiol. 68:1297-1304.
10. Cowles, C. E., and H. Goodrich-Blair. 2004. Characterization of a lipoprotein, NilC, required by Xenorhabdus nematophila for mutualism with its nematode host. Mol. Microbiol. 54:464-477.
11. Cowles, C. E., and H. Goodrich-Blair. 2006. nilR is necessary for co-ordinate repression of Xenorhabdus nematophila mutualism genes. Mol. Microbiol. 62:760-771.
12. Cowles, K. N., C. E. Cowles, G. R. Richards, E. C. Martens, and H. Goodrich-Blair. 2007. The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell. Microbiol. 9:1311-1323.
13. Cowles, K. N., and H. Goodrich-Blair. 2005. Expression and activity of a Xenorhabdus nematophila haemolysin required for full virulence towards Manduca sexta insects. Cell. Microbiol. 7:209-219.
14. Danese, P. N., G. R. Oliver, K. Barr, G. D. Bowman, P. D. Rick, and T. J. Silhavy. 1998. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J. Bacteriol. 180:5875-5884.
15. Danese, P. N., and T. J. Silhavy. 1997. The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev. 11:1183-1193.
16. Danese, P. N. , W. B. Snyder, C. L. Cosma, L. J. Davis, and T. J. Silhavy. 1995. The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev. 9:387-398.
17. Dartigalongue, C., and S. Raina. 1998. A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 17:3968-3980.
18. De Wulf, P., O. Kwon, and E. C. Lin. 1999. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J. Bacteriol. 181:6772-6778.
19. De Wulf, P., A. M. McGuire, X. Liu, and E. C. Lin. 2002. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J. Biol. Chem. 277:26652- 26661.
20. DiGiuseppe, P. A., and T. J. Silhavy. 2003. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185:2432-2440.
21. Dorel, C., O. Vidal, C. Prigent-Combaret, I. Vallet, and P. Lejeune. 1999. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett. 178:169-175.
22. Feldman, M., and G. Segal. 2004. A specific genomic location within the icm/dot pathogenesis region of different Legionella species encodes functionally similar but nonhomologous virulence proteins. Infect. Immun. 72:4503-4511.
23. Fernandez, L. A., and J. Berenguer. 2000. Secretion and assembly of regular surface structures in Gram-negative bacteria. FEMS Microbiol. Rev. 24: 21-44.
24. Forst, S., and B. Boylan. 2002. Characterization of the pleiotropic phenotype of an ompR strain of Xenorhabdus nematophila. Antonie Leeuwenhoek 81: 43-49.
25. Forst, S., and D. Clarke. 2002. Bacteria-nematode symbioses, p. 57-77. In R. Gaugier (ed.), Entomopathogenic nematology. CABI Publishing, Wallingford, United Kingdom.
26. Forst, S., B. Dowds, N. Boemare, and E. Stackebrandt. 1997. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51:47-72.
27. Forst, S., and K. Nealson. 1996. Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiol. Rev. 60:21-43.
28. Gal-Mor, O., and G. Segal. 2003. Identification of CpxR as a positive regulator of icm and dot virulence genes of Legionella pneumophila. J. Bacteriol. 185:4908-4919.
29. Gillespie, J. P., M. R. Kanost, and T. Trenczek. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42:611-643.
30. 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.
31. Goodrich-Blair, H., and D. J. Clarke. 2007. Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol. Microbiol. 64:260-268.
32. He, H., H. A. Snyder, and S. Forst. 2004. Unique organization and regulation of the mrx fimbrial operon in Xenorhabdus nematophila. Microbiology 150:1439-1446.
33. Herbert, E. E., and H. Goodrich-Blair. 2007. Friend and foe: the two faces of Xenorhabdus nematophila. Nat. Rev. Microbiol. 5:634-646.
34. Heungens, K., C. E. Cowles, and H. Goodrich-Blair. 2002. Identification of Xenorhabdus nematophila genes required for mutualistic colonization of Steinernema carpocapsae nematodes. Mol. Microbiol. 45:1337-1353.
35. Heusipp, G., K. M. Nelson, M. A. Schmidt, and V. L. Miller. 2004. Regulation of htrA expression in Yersinia enterocolitica. FEMS Microbiol. Lett. 231:227-235.
36. Humphreys, S., G. Rowley, A. Stevenson, M. F. Anjum, M. J. Woodward, S. Gilbert, J. Kormanec, and M. Roberts. 2004. Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infect. Immun. 72:4654-4661.
37. Hung, D. L., T. L. Raivio, C. H. Jones, T. J. Silhavy, and S. J. Hultgren. 2001. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20:1508-1518.
38. Ji, D., and Y. Kim. 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.
39. Jones, C. H., P. N. Danese, J. S. Pinkner, T. J. Silhavy, and S. J. Hultgren. 1997. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J. 16:6394-6406.
40. Jubelin, G., A. Vianney, C. Beloin, J. M. Ghigo, J. C. Lazzaroni, P. Lejeune, and C. Dorel. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187:2038-2049.
41. Kanost, M. R., H. Jiang, and X. Q. Yu. 2004. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 198:97-105.
42. Ledere, G. J., C. Tartera, and E. S. Metcalf. 1998. Environmental regulation of Salmonella typhi invasion-defective mutants. Infect. Immun. 66:682-691.
43. Martens, E. C., and H. Goodrich-Blair. 2005. The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation. Cell. Microbiol. 7:1723-1735.
44. Martens, E. C., K. Heungens, and H. Goodrich-Blair. 2003. Early colonization events in the mutualistic association between Steinernema carpocapsae nematodes and Xenorhabdus nematophila bacteria. J. Bacteriol. 185:3147-3154.
45. McBroom, A. J., and M. J. Kuehn. 2007. Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 63:545-558.
46. McCann, J., E. V. Stabb, D. S. Millikan, and E. G. Ruby. 2003. Population dynamics of Vibrio fischeri during infection of Euprymna scolopes. Appl. Environ. Microbiol. 69:5928-5934.
47. McCarter, L. L. 2006. Regulation of flagella. Curr. Opin. Microbiol. 9:180-186.
48. Mileykovskaya, E., and W. Dowhan. 1997. The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J. Bacteriol. 179:1029-1034.
49. Mitobe, J., E. Arakawa, and H. Watanabe. 2005. A sensor of the two-component system CpxA affects expression of the type III secretion system through posttranscriptional processing of InvE. J. Bacteriol. 187:107-113.
50. Nakayama, S., A Kushiro, T. Asahara, R. Tanaka, L. Hu, D. J. Kopecko, and H. Watanabe. 2003. Activation of hilA expression at low pH requires the signal sensor CpxA, but not the cognate response regulator CpxR, in Salmonella enterica serovar Typhimurium. Microbiology 149:2809-2817.
51. Nakayama, S. , and H. Watanabe. 1998. Identification of cpxR as a positive regulator essential for expression of the Shigella sonnei virF gene. J. Bacteriol. 180:3522-3528.
52. Nakayama, S., and H. Watanabe. 1995. Involvement of cpxA, a sensor of a two-component regulatory system, in the pH-dependent regulation of expression of Shigella sonnei virF gene. J. Bacteriol. 177:5062-5069.
53. Orchard, S. S., and H. Goodrich-Blair. 2004. Identification and functional characterization of a Xenorhabdus nematophila oligopeptide permease. Appl. Environ. Microbiol. 70:5621-5627.
54. Otto, K., and T. J. Silhavy. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. USA 99:2287-2292.
55. Park, D., and S. Forst. 2006. Co-regulation of motility, exoenzyme and antibiotic production by the EnvZ-OmpR-FlhDC-FliA pathway in Xenorhabdus nematophila. Mol. Microbiol. 61:1397-1412.
56. Park, Y., E. E. Herbert, C. E. Cowles, K. N. Cowles, M. L. Menard, S. S. Orchard, and H. Goodrich-Blair. 2007. Clonal variation in Xenorhabdus nematophila virulence and suppression of Manduca sexta immunity. Cell. Microbiol. 9:645-656.
57. Park, Y., and Y. Kim. 2000. Eicosanoids rescue Spodoptera exigua infected with Xenorhabdus nematophilus, the symbiotic bacteria to the entomopathogenic nematode Steinernema carpocapsae. J. Insect Physiol. 46:1469-1476.
58. Park, Y., Y. Kim, H. Tunaz, and D. W. Stanley. 2004. An entomopathogenic bacterium, Xenorhabdus nematophila, inhibits hemocytic phospholipase A2 (PLA2) in tobacco hornworms Manduca sexta. J. Invertebr. Pathol. 86:65-71.
59. Pogliano, J., A. S. Lynch, D. Belin, E. C. Lin, and J. Beckwith. 1997. Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev. 11:1169-1182.
60. Popiel, I., D. L. Grove, and M. J. Friedman. 1989. Infective juvenile formation in the insect parasitic nematode Steinernema feltiae. Parasitology 99:77-81.
61. Raivio, T. L. 2005. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol. Microbiol. 56:1119-1128.
62. Raivio, T. L., M. W. Laird, J. C. Joly, and T. J. Silhavy. 2000. Tethering of CpxP to the inner membrane prevents spheroplast induction of the Cpx envelope stress response. Mol. Microbiol. 37:1186-1197.
63. Raivio, T. L., D. L. Popkin, and T. J. Silhavy. 1999. The Cpx envelope stress response is controlled by amplification and feedback inhibition. J. Bacteriol. 181:5263-5272.
64. Raivio, T. L., and T. J. Silhavy. 2001. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:591-624.
65. E and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2:159-165.
66. Raivio, T. L., and T. J. Silhavy. 1997. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J. Bacteriol. 179:7724-7733.
67. R Development Core Team. 2006. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
68. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
69. Sauer, F. G., M. A. Mulvey, J. D. Schilling, J. J. Martinez, and S. J. Hultgren. 2000. Bacterial pili: molecular mechanisms of pathogenesis. Curr. Opin. Microbiol. 3:65-72.
70. Sicard, M., K. Brugirard-Ricaud, S. Pages, A. Lanois, N. E. Boemare, M. Brehelin, and A. Givaudan. 2004. Stages of infection during the tripartite interaction between Xenorhabdus nematophila, its nematode vector, and insect hosts. Appl. Environ. Microbiol. 70:6473-6480.
71. Sierra, G. 1957. A simple method for the detection of lipolytic activity of micro-organisms and some observations on the influence of the contact between cells and fatty substrates. Antonie Leeuwenhoek 23:15-22.
72. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-791.
73. Tapparel, C., A. Monod, and W. L. Kelley. 2006. The DNA-binding domain of the Escherichia coli CpxR two-component response regulator is constitutively active and cannot be fully attenuated by fused adjacent heterologous regulatory domains. Microbiology 152:431-441.
74. Vigneux, F., R. Zumbihl, G. Jubelin, C. Ribeiro, J. Poncet, S. Baghdiguian, A. Givaudan, and M. Brehelin. 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.
75. Vincent, C. D., B. A Buscher, J. R. Friedman, L. A. Williams, P. Bardill, and J. P. Vogel. 2006. Identification of non-dot/icm suppressors of the Legionella pneumophila ΔdotL lethality phenotype. J. Bacteriol. 188:8231-8243.
76. Visick, K. L., and L. M. Skoufos. 2001. Two-component sensor required for normal symbiotic colonization of Euprymna scolopes by Vibrio fischeri. J. Bacteriol. 183:835-842.
77. Vivas, E. I., and H. Goodrich-Blair. 2001. Xenorhabdus nematophilus as a model for host-bacterium interactions: rpoS is necessary for mutualism with nematodes. J. Bacteriol. 183:4687-4693.
78. Xu, J., and R. E. Hurlbert. 1990. Toxicity of irradiated media for Xenorhabdus spp. Appl. Environ. Microbiol. 56:815-818.
79. Yamamoto, K., and A. Ishihama. 2006. Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci. Biotechnol. Biochem. 70:1688-1695.