Chemosensory behaviors of parasites

Abstract

Many multicellular parasites seek out hosts by following trails of host-emitted chemicals. Host seeking is a characteristic of endoparasites such as parasitic worms as well as of ectoparasites such as mosquitoes and ticks. For host location, many of these parasites use CO(2), a respiration byproduct, in combination with host-specific chemicals. Recent work has begun to elucidate the behavioral responses of parasites to CO(2) and other host chemicals, and to unravel the mechanisms of these responses. Here we discuss recent findings that have greatly advanced our understanding of the chemosensory behaviors of host-seeking parasites. We focus primarily on well-studied parasites such as nematodes and insects, but also note broadly relevant findings in a few less well studied parasites.

Figure 1. Chemosensory responses of entomopathogenic nematodes (EPNs)

(a) Life cycle of EPNs. EPN IJs infect insect larvae either by entering through a natural body opening or by penetrating through the insect cuticle. IJs are associated with symbiotic bacteria, which they deposit into the host. The bacteria play an important role in overcoming the insect immune system. The nematodes develop and reproduce in the host cadaver for a few generations, feeding off the bacteria and digested insect tissue. New IJs then form and exit the cadaver to search for new hosts [106]. (b) IJs exiting a Galleria mellonella cadaver. Arrowhead indicates a clump of IJs; arrow indicates a single IJ. (c) The behavioral responses of H. bacteriophora IJs, S. carpocapsae IJs, and C. elegans dauers to the indicated odorants in a chemotaxis assay. The chemotaxis index ranges from 1 (perfect attraction) to −1 (perfect repulsion). Responses are color-coded according to the color scale on the lower right. (d) The odor response profiles of the EPNs are more similar to each other than to that of C. elegans despite their phylogenetic distance. Left, behavioral dendrogram of olfactory responses across species. Behavioral distance is based on the Euclidean distances between species based on their odor response profiles. Right, phylogenetic neighbor-joining tree. Branch lengths in the phylogenetic tree are proportional to genetic distances between taxa. Reprinted from [5] with permission. Abbreviations: EPNs, entomopathogenic nematodes; IJs, infective juveniles.

Figure 2. Representative schistosome life cycle

Eggs are passed in the urine or feces of the vertebrate host [49]. In the environment, the eggs hatch and release miracidia. Miracidia seek out snail hosts using temperature, gravity, light, and chemosensory cues; they then penetrate the snail. After multiple rounds of asexual reproduction in the snail, cercariae emerge from the snail and disperse. Cercariae orient themselves in the water column using temperature, gravity, and light [49]. When vertebrate hosts enter the water near cercariae, host skin compounds such as fatty acids and amino acids as well as warmth attract cercariae to the host and stimulate sustained attachment to and penetration of the host’s skin [49, 51, 53]. Within the host, cercariae use chemical gradients to guide migration to the intestines or bladder, pair, reproduce sexually, and lay eggs [54]. Some of the host-derived chemical cues for miracidia and cercariae are shown in red [, –53].

Figure 3. Odor coding by the An. gambiae AgOR repertoire

(a) Responses of AgORs to 110 odorants using the D. melanogaster ‘empty neuron’ system [76] for receptor decoding. The ‘empty neuron’ consists of an antennal olfactory neuron that lacks its endogenous odorant receptors. Odorant receptors of interest can be ectopically expressed in the ‘empty neuron’, and their odor responses can then be determined by single-unit electrophysiology [76]. AgOR response intensities are color-coded according to the scale on the right. (b) A comparison of An. gambiae and D. melanogaster odor space. For each species, the odor space is an n-dimensional space in which each axis represents the responses of one receptor in spikes/s, and n represents the total number of receptors tested. Each tested odorant was mapped to a particular position in this space based on the electrophysiological responses it elicited from each receptor in the ‘empty neuron’ system. To generate the graphs, principal component analysis was used to represent the n-dimensional odor spaces in three dimensions; the axes of the graphs correspond to the first three principle components. Left, An. gambiae odor space. Right, D. melanogaster odor space. Aromatics are more widely distributed in An. gambiae odor space, and esters are more widely distributed in D. melanogaster odor space. This suggests that mosquitoes may be better than fruit flies at discriminating among aromatics, some of which are emitted by human hosts, while fruit flies may be better at discriminating among esters, some of which are emitted by fruits. Reprinted from [77] with permission.

Figure 4. Some of the common olfactory cues used by multicellular parasites for host finding

Only odorants used by more than one family are shown. Many of the odorants listed are common in nature, so sources listed are representative but not exhaustive. Any chemical compound (R) containing a carboxyl group, as shown, is considered a carboxylic acid.