Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach

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.

Malaria Plasmodium agent induces alteration in the head proteome of their Anopheles mosquito host

“…Interestingly, two proteins revealed here have been demonstrated to be involved in behavioural modifications in other host-parasite systems. Tropomyosin has been shown to be involved in the behavioural manipulation of crustacean gammarids by acanthocephalans [16], while PGAM are involved in cricket behavioural manipulation induced by hairworms [15]. The comparison of proteins involved in behavioural modifications in different host-parasite systems raises the question of molecular convergence in manipulation processes.…”

“…An investigation of parasite-induced effects on host CNS proteome expression may play a crucial role in this respect [13], especially in insect vector-pathogen systems [14]. Proteomics, with the ability to investigate the translation of genomic information, offers an approach to study the global changes in protein expression of the host CNS caused by parasites [15][16][17]. Here, we have applied such an approach to the Anopheles gambiae-Plasmodium berghei (murine malaria) experimental model to elucidate the molecular mechanisms in the brain that underlie behavioural modifications.…”

Parasite manipulation of brain monoamines in California killifish ( Fundulus parvipinnis ) by the trematode Euhaplorchis californiensis

“…The manipulation of invertebrate hosts involves parasitesecreted molecules (Beckage 1993;de Jong-Brink et al 2001;Biron et al 2005), and neuroanatomical and monoaminergic disruption (Adamo & Shoemaker 2000;Helluy & Thomas 2003;Thomas et al 2003;Rojas & Ojeda 2005;Tain et al 2006), including reduced activity of monoaminergic neurons (Rosenberg et al 2006). There are fewer studies on vertebrates (see Klein (2003) for a review).…”

Proteomics of Anopheles gambiae

“…Interestingly, two proteins revealed in the study have been demonstrated to be involved in behavioural modifications in other hostparasite systems. Tropomyosin has been shown to be involved in the behavioural manipulation of crustacean gammarids by acanthocephalans [49], while phosphoglycerate mutase was involved in cricket behavioural manipulation induced by hairworms [50]. Furthermore, a heat shock response (HSP 20) and a variation of cytoarchitecture (tropomyosins) have been shown.…”