Dataset Information

Olfaction shapes host-parasite interactions in parasitic nematodes.

ABSTRACT: Many parasitic nematodes actively seek out hosts in which to 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. However, little is known about the olfactory cues that attract parasitic nematodes to hosts or the behavioral responses these cues elicit. Moreover, what little is known focuses on easily obtainable laboratory hosts rather than on natural or other ecologically relevant hosts. Here we investigate the olfactory responses of six diverse species of entomopathogenic nematodes (EPNs) to seven ecologically relevant potential invertebrate hosts, including one known natural host and other potential hosts collected from the environment. We show that EPNs respond differentially to the odor blends emitted by live potential hosts as well as to individual host-derived odorants. In addition, we show that EPNs use the universal host cue CO(2) as well as host-specific odorants for host location, but the relative importance of CO(2) versus host-specific odorants varies for different parasite-host combinations and for different host-seeking behaviors. We also identified host-derived odorants by gas chromatography-mass spectrometry and found that many of these odorants stimulate host-seeking behaviors in a species-specific manner. Taken together, our results demonstrate that parasitic nematodes have evolved specialized olfactory systems that likely contribute to appropriate host selection.

SUBMITTER: Dillman AR

PROVIDER: S-EPMC3435218 | biostudies-literature | 2012 Aug

REPOSITORIES: biostudies-literature

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Olfaction shapes host-parasite interactions in parasitic nematodes.

Dillman Adler R AR Guillermin Manon L ML Lee Joon Ha JH Kim Brian B Sternberg Paul W PW Hallem Elissa A EA

Proceedings of the National Academy of Sciences of the United States of America 20120731 35

Many parasitic nematodes actively seek out hosts in which to 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. However, little is known about the olfactory cues that attract parasitic nematodes to hosts or the behavioral responses these cues elicit. Moreover, what little is known focuses on easily obtainable laboratory hosts rather than on natural or other ecologically rel ...[more]

PMID: 22851767

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Project description:Signaling or communication between host and parasite may occur over relatively long ranges to enable host finding and acquisition by infective parasitic nematode larvae. Innate behaviors in infective larvae transmitted from the soil that enhance the likelihood of host contact, such as negative geotaxis and hypermotility, are likely mediated by mechanoreception and neuromuscular signaling. Host cues such as vibration of the substratum, elevated temperature, exhaled CO2, and other volatile odorants are perceived by mechanosensory and chemosensory neurons of the amphidial complex. Beyond this, the molecular systems that transduce these external cues within the worm are unknown at this time. Overall, the signal transduction mechanisms that regulate switching between dauer and continuous reproductive development in Caenorhabditis elegans, and doubtless other free-living nematodes, have provided a useful framework for testing hypotheses about how the morphogenesis and development of infective parasitic nematode larvae and the lifespan of adult parasites are regulated. In C. elegans, four major signal transduction pathways, G protein-coupled receptor signaling, insulin/insulin-like growth factor signaling, TGFβ-like signaling and steroid-nuclear hormone receptor signaling govern the switch between dauer and continuous development and regulate adult lifespan. Parasitic nematodes appear to have conserved the functions of G-protein-coupled signaling, insulin-like signaling and steroid-nuclear hormone receptor signaling to regulate larval development before and during the infective process. By contrast, TGFβ-like signaling appears to have been adapted for some other function, perhaps modulation of the host immune response. Of the three signal transduction pathways that appear to regulate development in parasitic nematodes, steroid-nuclear hormone signaling is the most straightforward to manipulate with administered small molecules and may form the basis of new chemotherapeutic strategies. Signaling between parasites and their hosts' immune systems also occurs and serves to modulate these responses to allow chronic infection and down regulate acute inflammatory responses. Knowledge of the precise nature of this signaling may form the basis of immunological interventions to protect against parasitism or related lesions and to alleviate inflammatory diseases of various etiologies.

Project description:Plant-parasitic nematodes are an important group of pests causing economic losses in agriculture worldwide. Among the plant-parasitic nematodes, the root-knot (Meloidogyne spp.) and root-lesion nematodes (Pratylenchus spp.) are considered the two most important ones affecting soybeans. In general, they damage soybean roots, causing a reduction of about one-third in productivity. The soil microbial community can exert a suppressive effect on the parasitism of plant-parasitic nematodes. Here, we investigated the effects of soil bacterial diversity on Meloidogyne javanica (Meloidogyne-assay) and Pratylenchus brachyurus (Pratylenchus-assay) suppression by manipulating microbial diversity using the dilution-to-extinction approach in two independent experiments under controlled conditions. Furthermore, we recorded the changes in the soil microbial community induced by plant-parasitic nematode infection. In Meloidogyne-assay, microbial diversity reduced the population density of M. javanica and improved plant performance. In Pratylenchus-assay, microbial diversity sustained the performance of soybean plants even at high levels of P. brachyurus parasitism. Each nematode population affected the relative abundance of different bacterial genera and altered the core microbiome of key groups within the bacterial community. Our findings provide fundamental insights into the interactions between soil bacterial diversity and plant-parasitic nematodes in soybean plants. IMPORTANCE Root-knot and root-lesion nematodes cause losses of billions of dollars every year to agriculture worldwide. Traditionally, they are controlled by using chemical nematicides, which in general have a negative impact on the environment and human health. Fortunately, the soil microbial community may suppress these pests, acting as an environmentally friendly alternative to control nematodes. However, the effects of soil microbial diversity on the parasitism of plant-parasitic nematodes still poorly understood. In this study, we provide fundamental insight into the interactions between soil bacterial diversity and plant-parasitic nematodes in soybean plants, which may be useful for the development of new strategies to control these phytopathogens.

Dataset Information

Olfaction shapes host-parasite interactions in parasitic nematodes.

Publications

Olfaction shapes host-parasite interactions in parasitic nematodes.

Similar Datasets

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