Acetylcholinesterase secreted by Anisakis simplex larvae (Nematoda: Anisakidae) parasitizing herring, Clupea harengus: an inverse relationship of enzyme activity in the host–parasite system

Magdalena Podolska,Katarzyna Nadolna

doi:10.1007/s00436-014-3878-9

Magdalena Podolska, Katarzyna Nadolna

Open Access

https://doi.org/10.1007/s00436-014-3878-9

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Abstract

Acetylcholinesterase (AChE) is a key enzyme involved in nerve impulse transmission in both vertebrates and invertebrates. In addition to neuromuscular AChE, many parasitic nematodes synthesize AChE in secretory glands and release the enzyme into their external environment. In this study, we evaluate the activities of both somatic and secreted AChE from larvae (L3) of the parasitic nematode Anisakis simplex, and compare these to the AChE activity in its host, herring, Clupea harengus. A. simplex larvae were obtained from a herring sampled in three areas of the southern Baltic. Enzyme kinetics were determined for excretory/secretory (E/S) products and somatic extracts of larvae as well as for herring muscle tissue. The results reveal that mean AChE activity is approximately fourfold higher in E/S products and eightfold higher in somatic extracts of post-secretory A. simplex larvae than in host muscle tissue. The level of AChE activity in nematodes is inversely related to the enzyme activity in their hosts, i.e. reduced AChE activity in herring was accompanied by increased enzyme activity in its parasites. The physiological function of AChE secreted by parasitic nematodes has been widely discussed in the literature, and numerous roles for this form of enzyme have been suggested. The results of our investigation indicate that AChE secretion by A. simplex larvae may constitute an adaptive mechanism that promotes survival under adverse environmental conditions. Larvae probably increase secretion of AChE in response to a direct and/or indirect effect of neurotoxic compounds. This is the first report of such a phenomenon in A. simplex.

Highlights

Cholinesterases are polymorphic enzymes involved in nerve impulse transmission in both vertebrates and invertebrates
The objective of the study was to test the hypothesis that AChE secreted by A. simplex larvae from herring determines the relationship observed between host and parasite AChE activity in areas of the Baltic polluted with neurotoxic compounds
Results of enzyme activity measurements indicated that the AChE level was much higher in A. simplex larvae than in herring host tissue and that an inverse relationship existed between enzyme activities of the host and its parasites (“mirror effect”)

Summary

Introduction

Cholinesterases are polymorphic enzymes involved in nerve impulse transmission in both vertebrates and invertebrates. In all invertebrates studied so far (i.e. nematodes and arthropods), the only cholinesterases found are of the AChE class (Toutant 1989; Combes et al 2000; Kang et al 2011a, b). Two different AChE genes have been defined in various arthropod species (Baxter and Barker 2002; Weill et al 2002, 2003; Lee et al 2006). Multiple forms of enzyme were identified in plant–parasitic nematodes: for example, three AChEs were defined in Heterodera glycines (Chang and Opperman 1992) and five in Meloidogyne incognita and Meloidogyne arenaria (Chang and Opperman 1991). Multiple forms of enzyme were identified in plant–parasitic nematodes: for example, three AChEs were defined in Heterodera glycines (Chang and Opperman 1992) and five in Meloidogyne incognita and Meloidogyne arenaria (Chang and Opperman 1991). Kang et al (2011a) found three AChEs in pinewood nematode Bursaphelenchus xylophilus, each with a distinct physiological function

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