Hostname: page-component-7dd5485656-hw7sx Total loading time: 0 Render date: 2025-10-31T05:35:01.073Z Has data issue: false hasContentIssue false
  • English
  • Français

Probing the tri-trophic interaction between insects, nematodes and Photorhabdus

Published online by Cambridge University Press:  26 May 2010

I. ELEFTHERIANOS ,
S. JOYCE ,
R. H. FFRENCH-CONSTANT ,
D. J. CLARKE  and
S. E. REYNOLDS
I. ELEFTHERIANOS*
Affiliation:
Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK Department of Biological Sciences, The George Washington University, Washington, D.C. 20052, USA
S. JOYCE
Affiliation:
Department of Microbiology, University College Cork, National University of Ireland, Cork, Ireland
R. H. FFRENCH-CONSTANT
Affiliation:
School of Biosciences, University of Exeter in Cornwall, Penryn TR10 9EZ, UK
D. J. CLARKE
Affiliation:
Department of Microbiology, University College Cork, National University of Ireland, Cork, Ireland
S. E. REYNOLDS
Affiliation:
Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK
*
*Corresponding author: Department of Biological Sciences and Institute for Biomedical Sciences, 336 Lisner Hall, 2023 G Street NW, The George Washington University, Washington DC 20052, USA. Tel: +202 994 0876. Fax: +202 994 6100. E-mail: ioannise@gwu.edu
Get access Rights & Permissions [Opens in a new window]

Summary

Photorhabdus sp. are entomopathogenic bacteria which, upon experimental infection, interact with the insect immune system, but little is known about the roles of their symbiotic nematode partners Heterorhabditis sp. in natural infections. Here, we investigated the respective contributions of nematodes and bacteria by examining humoral and cellular immune reactions of the model lepidopteran insect Manduca sexta against Heterorhabditis carrying Photorhabdus, nematodes free of bacteria (axenic nematodes) and bacteria alone. Insect mortality was slower following infection with axenic nematodes than when insects were infected with nematodes containing Photorhabdus, or the bacteria alone. Nematodes elicited host immune responses to a lesser extent than bacteria. Transcription of certain recognition and antibacterial genes was lower when insects were naturally infected with nematodes carrying no bacteria compared to insects that received bacteria, either with or without nematodes. Axenic nematodes also did not elicit such high levels of phenoloxidase activity and haemocyte aggregates as did treatments involving Photorhabdus. By contrast, the phagocytic capability of host haemocytes was decreased by both axenic and bacteria-associated nematodes, but not by Photorhabdus alone. These results imply that both bacteria and nematodes contribute separately to the pathogenic modulation of host immune responses during natural infections by the mutualistic Heterorhabdus-Photorhabdus complex.

Keywords

insect immunityManducaHeterorhabditisPhotorhabduscellular responsehumoral response

Information

Type
Research Article
Information
Parasitology , Volume 137 , Issue 11 , September 2010 , pp. 1695 - 1706
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

Au, C., Dean, P., Reynolds, S. E. and ffrench-Constant, R. H. (2004). Effect of the insect pathogenic bacterium Photorhabdus on insect phagocytes. Cellular Microbiology 6, 89–95.CrossRefGoogle ScholarPubMed
Brivio, M. F., Mastore, M. and Moro, M. (2004). The role of Steinernema feltiae body-surface lipids in host-parasite immunological interactions. Molecular and Biochemical Parasitology 135, 111–121.CrossRefGoogle ScholarPubMed
Brivio, M. F., Mastore, M. and Pagani, M. (2005). Parasite-host relationship: a lesson from a professional killer. Invertebrate Survival Journal 2, 41–53.Google Scholar
Brivio, M. F., Pagani, M. and Restelli, S. (2002). Immune suppression of Galleria mellonella (Insecta, Lepidoptera) humoral defenses induced by Steinernema feltiae (Nematoda, Rhabditida): involvement of the parasite cuticle. Experimental Parasitolgy 101, 149–156.CrossRefGoogle ScholarPubMed
Cerenius, L., Lee, B. L. and Söderhäll, K. (2008). The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29, 263–271.CrossRefGoogle ScholarPubMed
Ciche, T. A. and Ensign, J. C. (2003). For the insect pathogen, Photorhabdus luminescens, which end of a nematode is out? Applied Environmental Microbiology 69, 1890–1897.CrossRefGoogle ScholarPubMed
Daborn, P. J., Waterfield, N., Silva, C. P., Au, C. P., Sharma, S. and ffrench-Constant, R. H. (2002). A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proceedings of the National Academy of Sciences, USA 99, 10742–10747.CrossRefGoogle ScholarPubMed
Eleftherianos, I., Boundy, S., Joyce, S., Aslam, S., Marshall, J., Cox, R., Simpson, T., Clarke, D., ffrench-Constant, R. and Reynolds, S. (2007 a). An antibiotic produced by an insect-pathogenic bacterium suppresses host defenses through phenoloxidase inhibition. Proceedings of the National Academy of Sciences, USA 104, 2419–2424.CrossRefGoogle ScholarPubMed
Eleftherianos, I., Gökçen, F., Felföldi, G., Millichap, P. J., Trenczek, T. E., ffrench-Constant, R. H. and Reynolds, S. E. (2007 b). The immunoglobulin family protein Hemolin mediates cellular immune responses to bacteria in the insect Manduca sexta. Cellular Microbiology 9, 1137–1147.CrossRefGoogle ScholarPubMed
Eleftherianos, I., Marokhazi, J., Millichap, P. J., Hodgkinson, A. J., Sriboonlert, A., ffrench-Constant, R. H. and Reynolds, S. E. (2006 a). 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 Biochemistry and Molecular Biology 36, 517–525.CrossRefGoogle ScholarPubMed
Eleftherianos, I., Millichap, P. J., ffrench-Constant, R. H. and Reynolds, S. E. (2006 b). RNAi suppression of recognition protein mediated immune responses in the tobacco hornworm Manduca sexta causes increased susceptibility to the insect pathogen Photorhabdus. Developmental and Comparative Immunology 30, 1099–1107.CrossRefGoogle Scholar
Eleftherianos, I., Waterfield, N. R., Bone, P., Boundy, S., ffrench-Constant, R. H. and Reynolds, S. E. (2009). A single locus from the entomopathogenic bacterium Photorhabdus luminescens inhibits activated Manduca sexta phenoloxidase. FEMS Microbiology Letters 293, 170–176.CrossRefGoogle ScholarPubMed
Ferrandon, D., Imler, J.-L., Hetru, C. and Hoffmann, J. (2007). The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nature Reviews Immunology 7, 862–874.CrossRefGoogle ScholarPubMed
ffrench-Constant, R., Waterfield, N., Daborn, P., Joyce, S., Bennett, H., Au, C., Dowling, A., Boundy, S., Reynolds, S. and Clarke, D. (2003). Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiology Reviews 26, 433–456.CrossRefGoogle ScholarPubMed
Goodrich-Blair, H. and Clarke, D. J. (2007). Mutualism and pathogenesis in Xenorhabdus and Photorhabdus: two roads to the same destination. Molecular Microbiology 64, 260–268.CrossRefGoogle Scholar
Hallem, E. A., Rengarajan, M., Ciche, T. A. and Sternberg, P. W. (2007). Nematodes, bacteria, and flies: A tripartite model for nematode parasitism. Current Biology 17, 898–904.CrossRefGoogle Scholar
Han, R. C. and Ehlers, R. U. (2000). Pathogenicity, development, and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. Journal of Invertebrate Pathology 75, 55–58.CrossRefGoogle ScholarPubMed
Jiang, H., Wang, Y. and Kanost, M. R. (1996). Primary structure of ribosomal proteins S3 and S7 from Manduca sexta. Insect Molecular Biology 5, 31–38.CrossRefGoogle ScholarPubMed
Jiravanichpaisal, P., Lee, B. L. and Söderhall, K. (2006). Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211, 213–236.CrossRefGoogle ScholarPubMed
Joyce, S. A. and Clarke, D. J. (2003). A hexA homologue from Photorhabdus regulates pathogenicity, symbiosis and phenotypic variation. Molecular Microbiology 47, 1445–1457.CrossRefGoogle ScholarPubMed
Joyce, S. A., Watson, R. J. and Clarke, D. J. (2006). The regulation of pathogenicity and mutualism in Photorhabdus. Current Opinion in Microbiology 9, 127–132.CrossRefGoogle ScholarPubMed
Kanost, M. R., Jiang, H. and Yu, X. Q. (2004). Innate immune responses of a lepidopteran insect, Manduca sexta. Immunological Reviews 198, 97–105.CrossRefGoogle ScholarPubMed
Klowden, M. J. (2007). Circulatory systems. In Physiological Systems in Insects (ed. Klowden, M. J.), pp. 357–402. Academic Press, Boston, USA.Google Scholar
Lemaitre, B. and Hoffmann, J. (2007). The host defense of Drosophila melanogaster. Annual Review of Immunology 25, 697–743.CrossRefGoogle ScholarPubMed
Lowenberger, C. A., Ferdig, M. T., Bulet, P., Khalili, S., Hoffmann, J. A. and Christensen, B. M. (1996). Aedes aegypti: induced antibacterial proteins reduce the establishment and development of Brugia malayi. Experimental Parasitology 83, 191–201.CrossRefGoogle ScholarPubMed
Miller, J. S. and Stanley, D. W. (1998). The nodule formation reaction to bacterial infection: assessing the role of eicosanoids. In Techniques in Insect Immunology (ed. Weisner, A.), pp. 265–270. SOS Publications, Fair Haven, USA.Google Scholar
Nation, J. L. (2008). Circulatory system. In Insect Physiology and Biochemistry (ed. Nation, J. L.), pp. 339–365. CRC Press, Boca Raton, FL, USA.CrossRefGoogle Scholar
Reynolds, S. E., Nottingham, S. F. and Stephens, A. E. (1985). Food and water economy and its relation to growth in 5th-instar larvae of the tobacco hornworm, Manduca sexta. Journal of Insect Physiology 31, 119–127.CrossRefGoogle Scholar
Ribeiro, C., Duvic, B., Oliveira, P., Givauda, A., Palha, F., Simoes, N. and Brehélin, M. (1999). Insect immunity–effects of factors produced by a nematobacterial complex on immunocompetent cells. Journal of Insect Physiology 45, 677–685.CrossRefGoogle ScholarPubMed
Richman, A. and Kafatos, F. C. (1995). Immunity to eucaryotic parasites in vector insects. Current Opinion in Immunology 8, 14–19.CrossRefGoogle Scholar
Silva, C. P., Waterfield, N. R., Daborn, P. J., Dean, P., Chilver, T., Au, C. P. Y., Sharma, S., Potter, U., Reynolds, S. E. and ffrench-Constant, R. H. (2002). Bacterial infection of a model insect: Photorhabdus luminescens and Manduca sexta. Cellular Microbiology 4, 329–339.CrossRefGoogle Scholar
Strand, M. R. (2008). The insect cellular immune response. Insect Science 15, 1–14.CrossRefGoogle Scholar
Vallet-Gely, I., Lemaitre, B. and Boccard, F. (2008). Bacterial strategies to overcome insect defences. Nature Review Microbiology 6, 302–313.CrossRefGoogle ScholarPubMed
Vlisidou, I., Dowling, A. J., Evans, I. R., Waterfield, N., ffrench-Constant, R. H. and Wood, W. (2009). Drosophila embryos as model systems for monitoring bacterial infection in real time. PLOS Pathogens 5, e1000518.CrossRefGoogle ScholarPubMed
Wang, Y., Gaugler, R. and Cui, L. W. (1994). Variations in immune response of Popillia japonica and Acheta domesticus to Heterorhabditis bacteriophora and Steinernema species. Journal of Nematology 26, 11–18.Google ScholarPubMed
Wang, Y., Campbell, J. F. and Gaugler, R. (1995). Infection of entomopathogenic nematodes Steinernema glaseri and Heterorhabditis bacteriophora against Popillia japonica (Coleoptera, Scarabaeidae) larvae. Journal of Invertebrate Pathology 66, 178–184.CrossRefGoogle Scholar
Waterfield, N. R., Ciche, T. and Clarke, D. (2009). Photorhabdus and a host of hosts. Annual Review of Microbiology 63, 557–574.CrossRefGoogle Scholar
Watson, R. J., Joyce, S. A., Spencer, G. V. and Clarke, D. J. (2005). The exbD gene of Photorhabdus temperata is required for full virulence in insects and symbiosis with the nematode Heterorhabditis. Molecular Microbiology 56, 763–773.CrossRefGoogle ScholarPubMed
Willott, E., Trenczek, T., Thrower, L. W. and Kanost, M. R. (1994). Immunochemical identification of insect haemocyte populations: monoclonal antibodies distinguish four major haemocyte types in Manduca sexta. European Journal of Cellular Biology 65, 417–423.Google Scholar
Yu, X. Q., Zhu, Y. F., Ma, C., Fabrick, J. A. and Kanost, M. R. (2002). Pattern recognition proteins in Manduca sexta plasma. Insect Biochemistry and Molecular Biology 32, 1287–1293.CrossRefGoogle ScholarPubMed
Zhao, P., Li, J., Wang, Y. and Jiang, H. (2007). Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochemistry and Molecular Biology 37, 952–959.CrossRefGoogle ScholarPubMed