Parasitology

Research Article

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

I. ELEFTHERIANOSa1a2 c1, S. JOYCEa3, R. H. FFRENCH-CONSTANTa4, D. J. CLARKEa3 and S. E. REYNOLDSa1

a1 Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK

a2 Department of Biological Sciences, The George Washington University, Washington, D.C. 20052, USA

a3 Department of Microbiology, University College Cork, National University of Ireland, Cork, Ireland

a4 School of Biosciences, University of Exeter in Cornwall, Penryn TR10 9EZ, UK

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.

(Received October 31 2009)

(Revised February 24 2010)

(Accepted March 01 2010)

(Online publication May 26 2010)

Correspondence:

c1 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

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