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  • Review Article
  • Published:

Bacterial strategies to overcome insect defences

Key Points

  • This Review describes the crosstalk that exists between bacteria and insects, and, particularly, discusses the strategies that are used by bacterial pathogens to persist in insects and the responses of insects to such infections.

  • Insect infections can occur through different routes: bacteria can reach the haemolymph after wounding or assisted entry, but most of the interactions between insects and bacteria happen upon ingestion of contaminated food.

  • Only a handful of bacteria can persist in large numbers in the digestive tracts of insects. It is generally assumed that most ingested bacteria are eliminated from the gut environment by peristalsis or by other unknown mechanisms. The ability of bacteria to persist can be due to a single gene, and might be related to perturbation of gut physiology.

  • Bacteria that can persist after ingestion must overcome the insect immune response. The insect immune response occurs at the infection site in the gut, but some persisting bacteria can also trigger antimicrobial peptide production at the systemic level. Some entomopathogenic bacteria can evade the insect immune response, mainly by suppressing it.

  • Despite the characterization of multiple virulence factors, how pathogens kill insects is not known. Insect death results either from bacterial proliferation or from damages that are caused by a toxic factor (or factors). Multiple factors have been identified, and many of them are under the control of global regulatory systems.

  • In conclusion, it is becoming evident that bacterial infections of insect hosts involve crosstalk that is similar to the crosstalk that is required for bacterial infections of other metazoan hosts. The acquisition of determinants that allow bacteria to persist, or to counteract insect host defences, might change the host range of pathogens.

Abstract

Recent genetic and molecular analyses have revealed how several strategies enable bacteria to persist and overcome insect immune defences. Genetic and genomic tools that can be used with Drosophila melanogaster have enabled the characterization of the pathways that are used by insects to detect bacterial invaders and combat infection. Conservation of bacterial virulence factors and insect immune repertoires indicates that there are common strategies of host invasion and pathogen eradication. Long-term interactions of bacteria with insects might ensure efficient dissemination of pathogens to other hosts, including humans.

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Figure 1: Main routes of bacterial infection in insects.
Figure 2: Schematic diagram of local immune response in Drosophila.
Figure 3: Examples of bacterial infections in insects.

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References

  1. Boucias, D. G. & Pendland, J. C. Principles of Insect Pathology (Kluwer Academic Publishers, Dordrecht, 1998).

    Book  Google Scholar 

  2. Federici, B. A., Park, H. W., Bideshi, D. K., Wirth, M. C. & Johnson, J. J. Recombinant bacteria for mosquito control. J. Exp. Biol. 206, 3877–3885 (2003).

    Article  CAS  PubMed  Google Scholar 

  3. Aballay, A. & Ausubel, F. M. Caenorhabditis elegans as a host for the study of host–pathogen interactions. Curr. Opin. Microbiol. 5, 97–101 (2002).

    Article  CAS  PubMed  Google Scholar 

  4. Cosson, P. et al. Pseudomonas aeruginosa virulence analyzed in a Dictyostelium discoideum host system. J. Bacteriol. 184, 3027–3033 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rahme, L. G. et al. Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proc. Natl Acad. Sci. USA 94, 13245–13250 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Vodovar, N., Acosta, C., Lemaitre, B. & Boccard, F. Drosophila: a polyvalent model to decipher host–pathogen interactions. Trends Microbiol. 12, 235–242 (2004).

    Article  CAS  PubMed  Google Scholar 

  7. Clarkson, J. M. & Charnley, A. K. New insights into the mechanisms of fungal pathogenesis in insects. Trends Microbiol. 4, 197–203 (1996).

    Article  CAS  PubMed  Google Scholar 

  8. Baumann, P. & Moran, N. A. Non-cultivable microorganisms from symbiotic associations of insects and other hosts. Antonie Van Leeuwenhoek 72, 39–48 (1997).

    Article  CAS  PubMed  Google Scholar 

  9. Gil, R., Latorre, A. & Moya, A. Bacterial endosymbionts of insects: insights from comparative genomics. Environ. Microbiol. 6, 1109–1122 (2004).

    Article  CAS  PubMed  Google Scholar 

  10. Bulla, L. A., R. A., R. & St. Julian, G. Bacteria as insect pathogens. Annu. Rev. Microbiol. 29, 163–190 (1975).

    Article  CAS  PubMed  Google Scholar 

  11. Lysenko, O. Non-sporeforming bacteria pathogenic to insects: incidence and mechanisms. Annu. Rev. Microbiol. 39, 673–695 (1985).

    Article  CAS  PubMed  Google Scholar 

  12. Kobayashi, M. et al. Houseflies: not simple mechanical vectors of enterohemorrhagic Escherichia coli O157:H7. Am. J. Trop. Med. Hyg. 61, 625–629 (1999).

    Article  CAS  PubMed  Google Scholar 

  13. Douglas, A. E. & Beard, C. B. in Biology of the Insect Midgut (eds Lehane, M. J. & Billingsley, P. F.) (Chapman & Hall, London, 1996).

    Google Scholar 

  14. Kaslow, D. C. & Welburn, S. in Biology of the Insect Midgut (eds Lehane, M. J. & Billingsley, P. F.) (Chapman & Hall, London, 1996).

    Google Scholar 

  15. Pai, H. H., Chen, W. C. & Peng, C. F. Cockroaches as potential vectors of nosocomial infections. Infect. Control Hosp. Epidemiol. 25, 979–984 (2004).

    Article  PubMed  Google Scholar 

  16. Gage, K. L. & Kosoy, M. Y. Natural history of plague: perspectives from more than a century of research. Annu. Rev. Entomol. 50, 505–528 (2005).

    Article  CAS  PubMed  Google Scholar 

  17. Chapman, R. F. The Insects: Structure and Function (Cambridge University Press, Cambridge, 1998).

    Book  Google Scholar 

  18. Tzou, P. et al. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 13, 737–748 (2000).

    Article  CAS  PubMed  Google Scholar 

  19. Hao, Z., Kasumba, I. & Aksoy, S. Proventriculus (cardia) plays a crucial role in immunity in tsetse fly (Diptera: Glossinidiae). Insect Biochem. Mol. Biol. 33, 1155–1164 (2003).

    Article  CAS  PubMed  Google Scholar 

  20. Jarrett, C. O. et al. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Infect. Dis. 190, 783–792 (2004).

    Article  PubMed  Google Scholar 

  21. Ha, E. M., Oh, C. T., Bae, Y. S. & Lee, W. J. A direct role for dual oxidase in Drosophila gut immunity. Science 310, 847–850 (2005). Shows that dual oxidase is indispensable for gut antimicrobial activities in adult Drosophila.

    Article  CAS  PubMed  Google Scholar 

  22. Ha, E. M. et al. An antioxidant system required for host protection against gut infection in Drosophila. Dev. Cell 8, 125–132 (2005). Shows that homeostasis in redox balance modulates host survival after ingestion of bacteria.

    Article  CAS  PubMed  Google Scholar 

  23. Hinnebusch, B. J. et al. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296, 733–735 (2002). Identification of the gene that is responsible for gut persistence in fleas.

    Article  CAS  PubMed  Google Scholar 

  24. Perry, R. D., Pendrak, M. L. & Schuetze, P. Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis. J. Bacteriol. 172, 5929–5937 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Parsek, M. R. & Singh, P. K. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57, 677–701 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. Hinnebusch, B. J., Perry, R. D. & Schwan, T. G. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273, 367–370 (1996). Identification of the gene responsible for proventriculus colonization and digestive tract blockage.

    Article  CAS  PubMed  Google Scholar 

  27. Darby, C., Ananth, S. L., Tan, L. & Hinnebusch, B. J. Identification of gmhA, a Yersinia pestis gene required for flea blockage, by using a Caenorhabditis elegans biofilm system. Infect. Immun. 73, 7236–7242 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Flyg, C., Kenne, K. & Boman, H. G. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J. Gen. Microbiol. 120, 173–181 (1980).

    CAS  PubMed  Google Scholar 

  29. Chugani, S. A. et al. QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 98, 2752–2757 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Basset, A. et al. The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc. Natl Acad. Sci. USA 97, 3376–3381 (2000). First report of immune-response activation after ingestion of bacteria by Drosophila larvae.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Vodovar, N. et al. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc. Natl Acad. Sci. USA 102, 11414–11419 (2005). Characterization of P. entomophila pathogenicity in Drosophila.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Blow, N. S. et al. Vibrio cholerae infection of Drosophila melanogaster mimics the human disease cholera. PLoS Pathog. 1, e8 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Nehme, N. T. et al. A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog. 3, e173 (2007). Characterization of S. marcescens pathogenicity in Drosophila.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Kloepper, J. W., Brewer, J. W. & Harisson, M. D. Insect transmission of Erwinia carotovora var. carotovora and Erwinia carotovora var. atroseptica to potato plants in the field. Am. Potato. J. 58, 165–175 (1981).

    Article  Google Scholar 

  35. Molina, J. J., Harisson, M. D. & Brewer, J. W. Transmission of Erwinia carotovora var. atroseptica by Drosophila melanogaster meig. I. Acquisition and transmission of the bacterium. Am. Potato J. 54, 245–250 (1974).

    Article  Google Scholar 

  36. Basset, A., Tzou, P., Lemaitre, B. & Boccard, F. A single gene that promotes interaction of a phytopathogenic bacterium with its insect vector, Drosophila melanogaster. EMBO Rep. 4, 205–209 (2003). Identification of the gene that allows bacterial persistence in the Drosophila larval gut.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Acosta Muniz, C., Jaillard, D., Lemaitre, B. & Boccard, F. Erwinia carotovora Evf antagonizes the elimination of bacteria in the gut of Drosophila larvae. Cell. Microbiol. 9, 106–119 (2007).

    Article  PubMed  CAS  Google Scholar 

  38. Jackson, T. A., Boucias, D. G. & Thaler, J. O. Pathobiology of amber disease, caused by Serratia spp., in the New Zealand grass grub, Costelytra zealandica. J. Invertebr. Pathol. 78, 232–243 (2001).

    Article  CAS  PubMed  Google Scholar 

  39. Hurst, M. R. & Jackson, T. A. Use of the green fluorescent protein to monitor the fate of Serratia entomophila causing amber disease in the New Zealand grass grub, Costelytra zealandica. J. Microbiol. Methods 50, 1–8 (2002).

    Article  CAS  PubMed  Google Scholar 

  40. Hurst, M. R., Glare, T. R., Jackson, T. A. & Ronson, C. W. Plasmid-located pathogenicity determinants of Serratia entomophila, the causal agent of amber disease of grass grub, show similarity to the insecticidal toxins of Photorhabdus luminescens. J. Bacteriol. 182, 5127–5138 (2000). Identification of determinants responsible for Amber disease.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Grkovic, S., Glare, T. R., Jackson, T. A. & Corbett, G. E. Genes essential for amber disease in grass grubs are located on the large plasmid found in Serratia entomophila and Serratia proteamaculans. Appl. Environ. Microbiol. 61, 2218–2223 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Hurst, M. R., Glare, T. R. & Jackson, T. A. Cloning Serratia entomophila antifeeding genes — a putative defective prophage active against the grass grub Costelytra zealandica. J. Bacteriol. 186, 5116–5128 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hurst, M. R., Beard, S. S., Jackson, T. A. & Jones, S. M. Isolation and characterization of the Serratia entomophila antifeeding prophage. FEMS Microbiol. Lett. 270, 42–48 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. ffrench-Constant, R. H., Dowling, A. & Waterfield, N. R. Insecticidal toxins from Photorhabdus bacteria and their potential use in agriculture. Toxicon 49, 436–451 (2007).

    Article  CAS  PubMed  Google Scholar 

  45. Onfelt Tingvall, T., Roos, E. & Engstrom, Y. The imd gene is required for local Cecropin expression in Drosophila barrier epithelia. EMBO Rep. 2, 239–243 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Zaidman-Remy, A. et al. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24, 463–473 (2006).

    Article  CAS  PubMed  Google Scholar 

  47. Bischoff, V. et al. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog. 2, e14 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Ryu, J. H. et al. An essential complementary role of NF-κB pathway to microbicidal oxidants in Drosophila gut immunity. EMBO J. 25, 3693–3701 (2006). Shows that intestinal NF-κB- and AMP-dependent immunity is crucial to host survival against ROS-resistant bacteria.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Liehl, P., Blight, M., Vodovar, N., Boccard, F. & Lemaitre, B. Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. PLoS Pathog. 2, e56 (2006). Shows the importance of the bacterial metalloprotease AprA to counteract AMPs.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Vodovar, N. et al. Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nature Biotechnol. 24, 673–679 (2006).

    Article  CAS  Google Scholar 

  51. Leulier, F. et al. The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nature Immunol. 4, 478–484 (2003).

    Article  CAS  Google Scholar 

  52. Royet, J. & Dziarski, R. Peptidoglycan recognition proteins: pleiotropic sensors and effectors of antimicrobial defences. Nature Rev. Microbiol. 5, 264–277 (2007).

    Article  CAS  Google Scholar 

  53. Forst, S., Dowds, B., Boemare, N. & Stackebrandt, E. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu. Rev. Microbiol. 51, 47–72 (1997).

    Article  CAS  PubMed  Google Scholar 

  54. Goodrich-Blair, H. & Clarke, D. J. Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Mol. Microbiol. 64, 260–268 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. Hurst, G. D., Anbutsu, H., Kutsukake, M. & Fukatsu, T. Hidden from the host: Spiroplasma bacteria infecting Drosophila do not cause an immune response, but are suppressed by ectopic immune activation. Insect Mol. Biol. 12, 93–97 (2003). Host colonization by bacteria that avoid detection by the insect defences.

    Article  CAS  PubMed  Google Scholar 

  56. Herbert, E. E. & Goodrich-Blair, H. Friend and foe: the two faces of Xenorhabdus nematophila. Nature Rev. Microbiol. 5, 634–646 (2007).

    Article  CAS  Google Scholar 

  57. Ji, D. & Kim, Y. 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 (2004).

    Article  CAS  PubMed  Google Scholar 

  58. Apidianakis, Y. et al. Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression. Proc. Natl Acad. Sci. USA 102, 2573–2578 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Park, Y., Kim, Y., Putnam, S. M. & Stanley, D. W. The bacterium Xenorhabdus nematophilus depresses nodulation reactions to infection by inhibiting eicosanoid biosynthesis in tobacco hornworms, Manduca sexta. Arch. Insect Biochem. Physiol. 52, 71–80 (2003).

    Article  CAS  PubMed  Google Scholar 

  60. 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. 89, 258–264 (2005).

    Article  CAS  PubMed  Google Scholar 

  61. Eleftherianos, I., Millichap, P. J., ffrench-Constant, R. H. & Reynolds, S. E. 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. 30, 1099–1107 (2006). A small antibiotic molecule that is produced by Photorhabdus spp. acts as inhibitor of phenoloxidase in Manduca sexta.

    Article  CAS  PubMed  Google Scholar 

  62. Brugirard-Ricaud, K. et al. Site-specific antiphagocytic function of the Photorhabdus luminescens type III secretion system during insect colonization. Cell. Microbiol. 7, 363–371 (2005).

    Article  CAS  PubMed  Google Scholar 

  63. Eleftherianos, I. et al. An antibiotic produced by an insect-pathogenic bacterium suppresses host defenses through phenoloxidase inhibition. Proc. Natl Acad. Sci. USA 104, 2419–2424 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Haas, D. & Defago, G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Rev. Microbiol. 3, 307–319 (2005).

    Article  CAS  Google Scholar 

  65. Galan, J. E. & Collmer, A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322–1328 (1999).

    Article  CAS  PubMed  Google Scholar 

  66. Matsumoto, K. Role of bacterial proteases in pseudomonal and serratial keratitis. Biol. Chem. 385, 1007–1016 (2004).

    Article  CAS  PubMed  Google Scholar 

  67. Miyoshi, S. & Shinoda, S. Microbial metalloproteases and pathogenesis. Microbes Infect. 2, 91–98 (2000).

    Article  CAS  PubMed  Google Scholar 

  68. Travis, J., Potempa, J. & Maeda, H. Are bacterial proteinases pathogenic factors? Trends Microbiol. 3, 405–407 (1995).

    Article  CAS  PubMed  Google Scholar 

  69. ffrench-Constant, R. et al. Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol. Rev. 26, 433–456 (2003).

    Article  CAS  PubMed  Google Scholar 

  70. Bowen, D. J. et al. Genetic and biochemical characterization of PrtA, an RTX-like metalloprotease from Photorhabdus. Microbiology 149, 1581–1591 (2003).

    Article  CAS  PubMed  Google Scholar 

  71. Duchaud, E. et al. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nature Biotechnol. 21, 1307–1313 (2003).

    Article  CAS  Google Scholar 

  72. Derzelle, S. et al. The PhoP/PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J. Bacteriol. 186, 1270–1279 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Cowles, K. N., Cowles, C. E., Richards, G. R., Martens, E. C. & Goodrich-Blair, H. The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell. Microbiol. 9, 1311–1323 (2007).

    Article  CAS  PubMed  Google Scholar 

  74. Fedhila, S., Nel, P. & Lereclus, D. The InhA2 metalloprotease of Bacillus thuringiensis strain 407 is required for pathogenicity in insects infected via the oral route. J. Bacteriol. 184, 3296–3304 (2002). Demonstrates the involvement of metalloprotease in the pathogenesis of B. thuringiensis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Salamitou, S. et al. The plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 146, 2825–2832 (2000).

    Article  CAS  PubMed  Google Scholar 

  76. Titball, R. W., Hill, J., Lawton, D. G. & Brown, K. A. Yersinia pestis and plague. Biochem. Soc. Trans. 31, 104–107 (2003).

    Article  CAS  PubMed  Google Scholar 

  77. Waterfield, N. R., Wren, B. W. & Ffrench-Constant, R. H. Invertebrates as a source of emerging human pathogens. Nature Rev. Microbiol. 2, 833–841 (2004).

    Article  CAS  Google Scholar 

  78. Grenier, A. M., Duport, G., Pages, S., Condemine, G. & Rahbe, Y. The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl. Environ. Microbiol. 72, 1956–1965 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Dillon, R. J. & Dillon, V. M. The gut bacteria of insects: nonpathogenic interactions. Annu. Rev. Entomol. 49, 71–92 (2004).

    Article  CAS  PubMed  Google Scholar 

  80. Eleftherianos, I. et al. 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. 36, 517–525 (2006).

    Article  CAS  PubMed  Google Scholar 

  81. Tzou, P., Reichhart, J. M. & Lemaitre, B. Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants. Proc. Natl Acad. Sci. USA 99, 2152–2157 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Dimopoulos, G. Insect immunity and its implication in mosquito-malaria interactions. Cell. Microbiol. 5, 3–14 (2003).

    Article  CAS  PubMed  Google Scholar 

  83. Evans, J. D. et al. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645–656 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Zou, Z. et al. Comparative genomic analysis of the Tribolium immune system. Genome Biol. 8, R177 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Kanost, M. R., Jiang, H. & Yu, X. Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 198, 97–105 (2004).

    Article  CAS  PubMed  Google Scholar 

  86. Ryu, J. H. et al. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319, 777–782 (2008). Describes changes in the commensal community by modification of host innate immune homeostasis and protection from ingested pathogens by the microbiota.

    Article  CAS  PubMed  Google Scholar 

  87. Shirasu-Hiza, M. M. & Schneider, D. S. Confronting physiology: how do infected flies die? Cell. Microbiol. 9, 2775–2783 (2007). Characterization of the colonization process of Naucoris by M. ulcerans.

    Article  CAS  PubMed  Google Scholar 

  88. Marsollier, L. et al. Protection against Mycobacterium ulcerans lesion development by exposure to aquatic insect saliva. PLoS Med. 4, e64 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Marsollier, L. et al. Colonization of the salivary glands of Naucoris cimicoides by Mycobacterium ulcerans requires host plasmatocytes and a macrolide toxin, mycolactone. Cell. Microbiol. 7, 935–943 (2005).

    Article  CAS  PubMed  Google Scholar 

  90. Marsollier, L. et al. Aquatic insects as a vector for Mycobacterium ulcerans. Appl. Environ. Microbiol. 68, 4623–4628 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Marsollier, L. et al. Impact of Mycobacterium ulcerans biofilm on transmissibility to ecological niches and Buruli ulcer pathogenesis. PLoS Pathog. 3, e62 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  92. Brennan, C. A. & Anderson, K. V. Drosophila: the genetics of innate immune recognition and response. Annu. Rev. Immunol. 22, 457–483 (2004).

    Article  CAS  PubMed  Google Scholar 

  93. Lemaitre, B. & Hoffmann, J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25, 697–743 (2007).

    Article  CAS  PubMed  Google Scholar 

  94. Foley, E. & O'Farrell, P. H. Nitric oxide contributes to induction of innate immune responses to Gram-negative bacteria in Drosophila. Genes Dev. 17, 115–125 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Dijkers, P. & O'Farrell, P. H. Drosophila calcineurin promotes induction of innate immune responses. Curr. Biol. 17, 2087–2093 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Uvell, H. & Engstrom, Y. A multilayered defense against infection: combinatorial control of insect immune genes. Trends Genet. 23, 342–349 (2007).

    Article  CAS  PubMed  Google Scholar 

  97. Kocks, C. et al. Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123, 335–346 (2005).

    Article  CAS  PubMed  Google Scholar 

  98. Cerenius, L. & Soderhall, K. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198, 116–126 (2004).

    Article  CAS  PubMed  Google Scholar 

  99. Gillespie, J. P., Kanost, M. R. & Trenczek, T. Biological mediators of insect immunity. Annu. Rev. Entomol. 42, 611–643 (1997).

    Article  CAS  PubMed  Google Scholar 

  100. Hurst, G. D. & Jiggins, F. M. Male-killing bacteria in insects: mechanisms, incidence, and implications. Emerg. Infect. Dis. 6, 329–336 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. McGraw, E. A. & O'Neill, S. L. Wolbachia pipientis: intracellular infection and pathogenesis in Drosophila. Curr. Opin. Microbiol. 7, 67–70 (2004).

    Article  CAS  PubMed  Google Scholar 

  102. Dobson, S. L. et al. Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem. Mol. Biol. 29, 153–160 (1999).

    Article  CAS  PubMed  Google Scholar 

  103. Bourtzis, K., Pettigrew, M. M. & O'Neill, S. L. Wolbachia neither induces nor suppresses transcripts encoding antimicrobial peptides. Insect Mol. Biol. 9, 635–639 (2000).

    Article  CAS  PubMed  Google Scholar 

  104. Min., K. T. & Benzer, S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl Acad. Sci. USA 94, 10792–10796 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Priest, F. G. in Entomopathogenic Bacteria: From Laboratory to Field Application (eds Charles, J.-F., Delécluse, A. & Nielsen-LeRoux, C.) 1–22 (Kluwer Academic Publishers, Dordrecht, 2000).

    Book  Google Scholar 

  106. Bravo, A., Gill, S. S. & Soberon, M. Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49, 423–435 (2007).

    Article  CAS  PubMed  Google Scholar 

  107. de Maagd, R. A., Bravo, A., Berry, C., Crickmore, N. & Schnepf, H. E. Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu. Rev. Genet. 37, 409–433 (2003).

    Article  CAS  PubMed  Google Scholar 

  108. Schnepf, E. et al. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62, 775–806 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Aronson, A. I. & Shai, Y. Why Bacillus thuringiensis insecticidal toxins are so effective: unique features of their mode of action. FEMS Microbiol. Lett. 195, 1–8 (2001).

    Article  CAS  PubMed  Google Scholar 

  110. Peferoen, M. Progress and prospects for field use of Bt genes in crops. TIBTech, 173–177 (1997).

    Article  CAS  Google Scholar 

  111. Hansen, B. M. & Salamitou, S. in Entomopathogenic Bacteria: From Laboratory to Field Application (eds Charles, J.-F., Delécluse, A. & Nielsen-LeRoux, C.) 41–64 (Kluwer Academic Publishers, Dordrecht, 2000).

    Book  Google Scholar 

  112. Broderick, N. A., Raffa, K. F. & Handelsman, J. Midgut bacteria required for Bacillus thuringiensis insecticidal activity. Proc. Natl Acad. Sci. USA 103, 15196–15199 (2006). Demonstrates that commensal bacteria are required to kill gypsy moth upon B. thuringiensis infection.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Harada, H. & Ishikawa, H. Experimental pathogenicity of Erwinia aphidicola to pea aphid, Acyrthosiphon pisum. J. Gen. Appl. Microbiol. 43, 363–367 (1997).

    Article  CAS  PubMed  Google Scholar 

  114. Fedhila, S., Daou, N., Lereclus, D. & Nielsen-LeRoux, C. Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects. Mol. Microbiol. 62, 339–355 (2006).

    Article  CAS  PubMed  Google Scholar 

  115. Rolain, J. M., Franc, M., Davoust, B. & Raoult, D. Molecular detection of Bartonella quintana, B. koehlerae, B. henselae, B. clarridgeiae, Rickettsia felis, and Wolbachia pipientis in cat fleas, France. Emerg. Infect. Dis. 9, 338–342 (2003).

    Article  CAS  PubMed  Google Scholar 

  116. Bowen, D. et al. Insecticidal toxins from the bacterium Photorhabdus luminescens. Science 280, 2129–2132 (1998). Identification of Tc-toxins.

    Article  CAS  PubMed  Google Scholar 

  117. Morgan, J. A., Sergeant, M., Ellis, D., Ousley, M. & Jarrett, P. Sequence analysis of insecticidal genes from Xenorhabdus nematophilus PMFI296. Appl. Environ. Microbiol. 67, 2062–2069 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Waterfield, N. R., Bowen, D. J., Fetherston, J. D., Perry, R. D. & ffrench-Constant, R. H. The tc genes of Photorhabdus: a growing family. Trends Microbiol. 9, 185–191 (2001).

    Article  CAS  PubMed  Google Scholar 

  119. Charles, J. F., Silva-Filha, M.-H. & Nielsen-LeRoux, C. in Entomopathogenic Bacteria: From Laboratory to Field Application (eds Charles, J. F., Delécluse, A. & Nielsen-LeRoux, C.) 237–252 (Kluwer Academic Press, Dordrecht, 2000).

    Book  Google Scholar 

  120. Daborn, P. J. et al. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc. Natl Acad. Sci. USA 99, 10742–10747 (2002). Identification of the Mcf toxin.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank F. Leulier, N. Vodovar and C. Nielsen-LeRoux for helpful discussions and critical reading of the manuscript. Work described in this Review that was performed in our laboratories was supported by Centre National de la Recherche Scientifique (CNRS), Agence Nationale de la Recherche, the Schlumberger and Bettancourt Foundations, and the Association 'Vaincre la Mucoviscidose'.

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Correspondence to Frédéric Boccard.

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DATABASES

Entrez Genome Project

Bacillus cereus

Bacillus thuringiensis

Mycobacterium ulcerans

Photorhabdus luminescens

Pseudomonas entomophila

Serratia marcescens

Yersinia pestis

FURTHER INFORMATION

Bruno Lemaitre's homepage

Bruno Lemaitre's homepage

Frédéric Boccard's homepage

Glossary

Persistence

The survival of bacteria in large numbers in a host.

Colonization

The ability to multiply in the host.

Innate immunity

Effector mechanisms that control infection and that possess a certain degree of specificity to different classes of microorganisms.

Biofilm

Association of bacteria to form a structured community, in contrast to free-living, planktonic bacteria.

Pathogenic

The ability to cause damage to a host.

Tc-toxin

Insecticidal toxin complex, originally characterized in Photorhabdus and Xenorhabdus species.

Peptidoglycan recognition proteins

Peptidoglycan recognition proteins are innate immunity molecules that are present in most invertebrate and vertebrate animals.

Infectious

The ability to colonize a host and induce the host immune response.

Type III secretion system

A secretion apparatus that allows direct injection of effectors from bacteria into host cells.

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Vallet-Gely, I., Lemaitre, B. & Boccard, F. Bacterial strategies to overcome insect defences. Nat Rev Microbiol 6, 302–313 (2008). https://doi.org/10.1038/nrmicro1870

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