Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach

Author:

Biron D.G1,Marché L2,Ponton F1,Loxdale H.D3,Galéotti N4,Renault L2,Joly C1,Thomas F1

Affiliation:

1. GEMI, UMR CNRS/IRD 2724IRD, 911 av. Agropolis BP 64501, 34394 Montpellier cedex 5, France

2. INRA, UMR BiO3P, Domaine de la Motte, BP 3532735653 Le Rheu cedex, France

3. Plant and Invertebrate Ecology Division, Rothamsted ResearchHarpenden, Hertfordshire AL5 2JQ, UK

4. LGF 2580-CNRS, LGF 2580-CNRS141 rue de la Cardonille, 34094 Montpellier cedex 5, France

Abstract

Abstract The parasitic Nematomorph hairworm, Spinochordodes tellinii (Camerano) develops inside the terrestrial grasshopper, Meconema thalassinum (De Geer) (Orthoptera: Tettigoniidae), changing the insect's responses to water. The resulting aberrant behaviour makes infected insects more likely to jump into an aquatic environment where the adult parasite reproduces. We used proteomics tools (i.e. two-dimensional gel electrophoresis (2-DE), computer assisted comparative analysis of host and parasite protein spots and MALDI-TOF mass spectrometry) to identify these proteins and to explore the mechanisms underlying this subtle behavioural modification. We characterized simultaneously the host (brain) and the parasite proteomes at three stages of the manipulative process, i.e. before, during and after manipulation. For the host, there was a differential proteomic expression in relation to different effects such as the circadian cycle, the parasitic status, the manipulative period itself, and worm emergence. For the parasite, a differential proteomics expression allowed characterization of the parasitic and the free-living stages, the manipulative period and the emergence of the worm from the host. The findings suggest that the adult worm alters the normal functions of the grasshopper's central nervous system (CNS) by producing certain ‘effective’ molecules. In addition, in the brain of manipulated insects, there was found to be a differential expression of proteins specifically linked to neurotransmitter activities. The evidence obtained also suggested that the parasite produces molecules from the family Wnt acting directly on the development of the CNS. These proteins show important similarities with those known in other insects, suggesting a case of molecular mimicry. Finally, we found many proteins in the host's CNS as well as in the parasite for which the function(s) are still unknown in the published literature (www) protein databases. These results support the hypothesis that host behavioural changes are mediated by a mix of direct and indirect chemical manipulation.

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

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