Fundam, appl, NemalOl" 1993, 16 (3), 193-198 Fomm article CHEMOSENSORY PHYSIOLOGY OF NEMATODES Jens AuMANN !nslilute ofPhylopalhology, University of Kiel, Hermann-Rodewald-Slrasse 9, 2300 Kiel l, Germany, Accepted for publication 20 October 1992, Key-words: Nematodes, chemosensory physiology, chemoreception, transduction, transmission, Little is yet known about the subject of this paper. Morphology and distribution of nematode cht. Several sciences like deve!opmental biology have profit­ mosensilla ed from the use of Caenorhabditis elegans as a mode! (Wood, 1988), Although the neuroanatomy of nema­ Nematode chemosensilla are composed of neurons, todes has been weil examined in this model, the neu­ gland cells and supporting cells. The neurons connect rosciences made progress with other animals, The se­ the outer surface with the nerve ring, Their dendritic quencing of the C. elegans genome as part of the Human nerve extensions are located in body pores and are thus Genome Project (Sulston el al., 1992) may, however, in contact with the external environment. The pores are lead to the structural and functional identification of filled with exudates that are produced in gland cells. many yet unknown molecules, and our knowledge of the Using these criteria, several sensilla can be cIassified as physiological processes involved in the recognition of chemosensitive. In the anterior region, amphids are gen­ chernical stimuli in nematodes may progress rapidly. erally considered to have a chemosensitive function. Other approaches appear more complicated. Despite Other anterior sensilla inside body pores with the same successful attempts by Jones el al. (1991) to record elec­ function are the inner labial sensilla, the outer labial trical activity of chemosensory neurons in nematodes, sensilla and the cephalic sensilla. In the posterior region, difficulties in the application of electrophysiological the phasmids of the Secernentea and the spicule recep­ methods are imposed by the small size of plant-parasitic tors of males probably act as chemosensilla. Nematode and free-living nematodes and by the preparation of chemosensilla have been described in detail (McLaren, suitable environmental conditions for animal-parasitic 1976a, b; Coomans, 1979; Wright, 1980, 1983; and species. Coomans & De Grisse, 1981), whereas Chalfie and The senses of taste and smell can be differentiated in White (1988) confined their description to C, elegans. vertebrates and in insects, but this differentiation ap­ A model ofvertebrate and insect olfaction pears meaningless for animais like nematodes that live in aquatic habitats (Schmidt-Nielsen, 1990). 1 will there­ The following model is based on various publications fore use the terms " chemosensilla " for the chemical (Augustine el al., 1987; Vogt el al., 1990; Bruch, 1990; sense organs and" chemosensitive " for their function. Burchell, 1991; Korsching, 1991) according to which The foIlowing paragraphs fust describe briefly the olfactory signaIs bind to the extracellular side of trans­ morphology and distribution of nematode chemosen­ membrane receptor proteins of dendritic nerve exten­ silla and present a model of vertebrate and insect olfac­ sions after they have passed the mucus layer of the ver­ tion. The conformity of this model with our present tebrate olfactory epithelium or the insect sensillum knowledge of nematode chemosensory physiology is Iymph. Binding is followed by the dissociation of the then discussed in the next five paragraphs. They are signal molecules from their receptors. The receptor pro­ arranged in the sequence of events that start with the teins activate G (or guanosine triphosphate-binding) diffusion of signal molecules into the chemosensillum­ proteins on the inner side of the cell membrane, which in associated exudates, i.e. pre-interactive events, receptor turn activate enzymes (adenylate cyclase or phospholi­ events, post-interactive events, transduction, and trans­ pase C) that catalyze the fonnation of secondary mess­ mission. Finally, the prospects for nematode control are engers (cyclic AMP or inositol trisphosphate, respec­ outlined from the data and hypotheses presented in the tively), These messengers then open secondary preceeding paragraphs. This paper is based on an idea messenger-gated ion channels. A rapid ion flux through expressed by Dodd and Castellucci (1991) :" ... ail sen­ the channels changes the e!ectric potential on the mem­ sory systems rely on the same basic principles of proc­ brane surface. This causes the opening of voltage-gated essing and organization not only in humans, but ion channe!s and the generation of an action potential. throughout much of phylogeny, " When the action potential has arrived at the chernical /SSN 1164-5571193/031l 93 06 S 2.60/ © Gaulhie1'-Villars - ORSTOM 193 r- l 2 HAl 1993 J. Aumann synapse between the sensory neuron and a neighbouring Receptor events 2 2 neuron, Ca +-channels are opened. The Ca +influx near Odorant receptor mo1ecules were probably identified the synapse causes the secretion of neurotransmitters at for the first time by Buck and Axel (1991). They the presynaptic side of the synaptic cleft. They bind to showed that these molecules from rat olfactory tissue receptors at the postsynaptic side of the cleft. Finally the belong to a family of G protein-coupled receptor pro­ animal reacts to the olfactory signal, for instance by the teins with seven trans-membrane spanning regions. One activation of motoneurons. of the most intensively studied members of this family is the 13-adrenergic receptor of vertebrates (Kobilka, Pre-interactive events 1992). Nematode receptor molecu]es are probably located In vertebrates and insects, the passage of hydrophobic on the surface of the dendritic nerve extensions of che­ olfactory signais through the aqueous mucus layer of the mosensilla. Little is known about their properties Gans­ vertebrate olfactory epithelium or through the aqueous son, 1987). Lectins, more or less specific carbohydrate­ insect sensillum Iymph may be aided by the binding of binding proteins or glycoproteins, have been shown to the signais to olfactory binding proteins, e.g. the odor­ inhibit the recognition of chemical signals in P. redivivus ant-binding proteins (OBP) of vertebrates and the phe­ Gansson & Nordbring-Hertz, 1984), C. elegans Geya­ romone-binding proteins (PBP) of insects (Carr el al., prakash el al., 1985) and Trichoslrongylus colubriformis 1990; Getchell & Getchell, 1990; Lerner el al., 1990; (Bone & Bottjer, 1985). It was assumed that inhibition Pelosi & Maida, 1990; Pevsner & Snyder, 1990). In ne­ resulted from lectin binding to receptor molecules, in­ matodes, however, signal molecules appear to be hydro­ dicating the occurrence of carbohydrate chains in these philic, because these animais live in aqueous environ­ molecules Gansson, 1987). However, the recognition of ments. Molecules with a function similar to the odorant­ chemical signais by males of Helerodera schachlii could and pheromone-binding proteins of vertebrates and not be inhibited by lectins (Aumann el al., 1990). These insects, respectively, therefore seem to be useless for ne­ differences between species are confirmed by the obser­ matodes. Neverthe1ess, this question is still unresolved, vation of Aumann and Wyss (1992) that severa] lectins since results of Jones el al. (1992) indicate that genes diffused into the amphidial pores of P. redivivus but not coding for proteins similar to insect olfactory binding of H. schachlii. An inhibition of chemorecognition of proteins are present in nematodes. H. schachlii males after treatrnent with the extracellulari­ The composition of gland cell-secreted exudates fill­ Iy acting sulfhydryl reagent mersalyl acid points to the ing the pores of nematode chemosensilla is important, occurrence of disulfide bridges in these molecules (Au­ because signal molecules have to pass the exudates on mann, 1991). Chalfie and Wolinsky (1990) suggested their way toward the receptors. These exudates have that the deg-l gene of C. elegans may encode ion chan­ been identified as glycoproteins in the amphids of Hele­ nels or membrane receptors in the nervous system. rodera schachlii males (Aumann, 1989). Several exper­ iments with other species from ail major trophic groups Post-interactive events have shown that lectins bind specifical!y to the exudates (Forrest & Robertson, 1986; McClure & Stynes, 1988; After binding of signais and the fol!owing transduc­ Aumann & Wyss, 1989; Aumann el al., 1991; Ibrahim, tion, a signal accumulation in the chemosensillum-asso­ 1991) or in the pore region of chemosensilla (Bowman ciated exudates has to be prevented; otherwise a sensi­ el al., 1988; Davis el a!., 1988; Forrest el al., 1988a, b; tive recognition of concentration gradients is not Bird el al., 1989; Robertson el al., 1989), indicating that guarameed (Stengl el al., 1992). Several mechanisms the sensillum exudates contain carbohydrates. It was preventing an accumulation of odorants have been dis­ postulated that sorne of these carbohydrates are sialic cussed : i) uptake into the vertebrate olfactory epitheli­ acids with a function in chemoreception (e.g. Zucker­ um and a subsequent enzymatic degradation (Lazard el man, 1983). They have been proposed to occur at the al., 1991); il) enzymatic degradation in the insect sensil­ chemosensilla of Panagrellus redivivus Gansson lum Iymph r:vogt el al., 1985); iil) binding to phero­ & N ordbring-Hertz, 1983, 1984) and Melozdogyne spp. mone-binding proteins