Host-Seeking, Olfaction, Foraging Strategies, and the Genomic Architecture of Parasitisim among Steinernema Nematodes

Abstract

Many parasitic nematodes actively seek out hosts to infect and thus complete their lifecycles. Olfaction is thought to play an important role in the host-seeking process, with parasites following a chemical trail toward host-associated odors. Steinernema is a diverse genus of entomopathogenic nematodes, with over 60 described species. The host-seeking behaviors of Steinernema include chemotaxis and jumping behavior and vary along a foraging strategy continuum between cruise and ambush strategies. Little is known about the odors that stimulate host-seeking behavior or how olfactory information is interpreted in these agriculturally important parasitic nematodes. We explored the host-seeking responses of several Steinernema species to CO_2 and volatile organic compounds produced by laboratory and ecologically relevant potential hosts. We show that all Steinernema species tested are attracted to CO_2, but display varying behavioral responses to different potential hosts, suggesting that they can differentiate between potential hosts based on odor alone. CO_2 seems to play a key role in the host-seeking process for steinernematids, though this varies for different parasite-host combinations and for different host-seeking behaviors. Further, we used gas chromatography-mass spectrometry and solid-phase microextractiongas chromatography-mass spectrometry to identify odorants emitted by seven potential hosts. We found that these odorants stimulate host-seeking behaviors in a species-specific manner, suggesting that parasitic nematodes have evolved highly specialized olfactory systems to enable their navigation through complex environments and make appropriate host selection decisions. To pursue these observations further, we sequenced the genomes and transcriptomes of five Steinernema species (S. carpocapsae, S. scapterisci, S. monticolum, S. feltiae, and S. glaseri). In an unbiased search through the vast genomic data, we found striking evidence of expansions in protease, protease inhibitor, and G-protein coupled receptor families. Our results indicate that Steinernema species have experienced significant evolution of these protein families, provocatively suggesting that the repertoire of olfactory receptors and armory of proteases underlie niche partitioning and the evolution of foraging strategy and host range among Steinernema nematodes.

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