Host orientation using volatiles in the phoretic nematode <i>Caenorhabditis japonica</i>

Okumura, Etsuko; Yoshiga, Toyoshi

doi:10.1242/jeb.105353

Cited by 12 publications

(5 citation statements)

References 24 publications

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“…It has been shown that dauer stage Caenorhabditis spp. are attracted to certain insect species, increasing the opportunity to engage in phoresis [57]. This cluster of shared srsx GPCRs may therefore mediate this attraction, in isolation, or in synergy with other such receptors.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional variation and divergence of host-finding behaviour in Steinernema carpocapsae infective juveniles

et al. 2019

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BackgroundSteinernema carpocapsae is an entomopathogenic nematode that employs nictation and jumping behaviours to find potential insect hosts. Here we aimed to investigate the transcriptional basis of variant host-finding behaviours in the infective juvenile (IJ) stage of three S. carpocapsae strains (ALL, Breton and UK1), with a focus on neuronal genes known to influence behaviour in other nematode species. Identifying gene expression changes that correlate with variant host-finding behaviours will further our understanding of nematode biology.ResultsRNA-seq analysis revealed that whilst up to 28% of the S. carpocapsae transcriptome was differentially expressed (P < 0.0001) between strains, remarkably few of the most highly differentially expressed genes (> 2 log2 fold change, P < 0.0001) were from neuronal gene families. S. carpocapsae Breton displays increased chemotaxis toward the laboratory host Galleria mellonella, relative to the other strains. This correlates with the up-regulation of four srsx chemosensory GPCR genes, and a sodium transporter gene, asic-2, relative to both ALL and UK1 strains. The UK1 strain exhibits a decreased nictation phenotype relative to ALL and Breton strains, which correlates with co-ordinate up-regulation of neuropeptide like protein 36 (nlp-36), and down-regulation of an srt family GPCR gene, and a distinct asic-2-like sodium channel paralogue. To further investigate the link between transcriptional regulation and behavioural variation, we sequenced microRNAs across IJs of each strain. We have identified 283 high confidence microRNA genes, yielding 321 predicted mature microRNAs in S. carpocapsae, and find that up to 36% of microRNAs are differentially expressed (P < 0.0001) between strains. Many of the most highly differentially expressed microRNAs (> 2 log2 fold, P < 0.0001) are predicted to regulate a variety of neuronal genes that may contribute to variant host-finding behaviours. We have also found evidence for differential gene isoform usage between strains, which alters predicted microRNA interactions, and could contribute to the diversification of behaviour.ConclusionsThese data provide insight to the transcriptional basis of behavioural variation in S. carpocapsae, supporting efforts to understand the molecular basis of complex behaviours in nematodes.

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Section: Discussionmentioning

confidence: 99%

Transcriptional variation and divergence of host-finding behaviour in Steinernema carpocapsae infective juveniles

et al. 2019

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“…Thus, it is possible that new habitat and substrate types will be discovered in the future, especially if sampling efforts go beyond France, Germany, the UK, and the US, where most previous collections were made. Compared to other Caenorhabditis species such as C. japonica (Yoshiga et al 2013; Okumura and Yoshiga 2014) or C. drosophilae (Kiontke 1997), the species C. elegans does not appear to have a highly specialized habitat nor a highly specialized biotic association with larger invertebrates. Although much remains to be discovered, C. elegans seems to have a more generalist lifestyle, which appears similar to that of some other Caenorhabditis species such as C. briggsae or C. remanei (see possible competition relationships in Possible competitors ).…”

Section: Habitats and Substratesmentioning

confidence: 95%

“…, feeding on the decomposing host after it dies) underlies the association (Kiontke and Sudhaus 2006). More specific relationships with invertebrate hosts are known, for example for the nematode Pristionchus pacificus , which in part lives in association with scarab beetles (Sommer and McGaughran 2013), or C. japonica , which shows a phoretic interaction with the bug Parastrachia japonensis (Yoshiga et al 2013; Okumura and Yoshiga 2014). In the case of C. elegans , more details on the specificity of the interaction would now require specially designed studies, such as life history assays on the host or collection of dead hosts from the wild (beyond one anecdotal report in Barrière and Félix 2007).…”

Section: Macroscopic Invertebrates As Possible Vectors or Hostsmentioning

confidence: 99%

The Natural Biotic Environment ofCaenorhabditis elegans

2017

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Organisms evolve in response to their natural environment. Consideration of natural ecological parameters are thus of key importance for our understanding of an organism’s biology. Curiously, the natural ecology of the model species Caenorhabditis elegans has long been neglected, even though this nematode has become one of the most intensively studied models in biological research. This lack of interest changed ∼10 yr ago. Since then, an increasing number of studies have focused on the nematode’s natural ecology. Yet many unknowns still remain. Here, we provide an overview of the currently available information on the natural environment of C. elegans. We focus on the biotic environment, which is usually less predictable and thus can create high selective constraints that are likely to have had a strong impact on C. elegans evolution. This nematode is particularly abundant in microbe-rich environments, especially rotting plant matter such as decomposing fruits and stems. In this environment, it is part of a complex interaction network, which is particularly shaped by a species-rich microbial community. These microbes can be food, part of a beneficial gut microbiome, parasites and pathogens, and possibly competitors. C. elegans is additionally confronted with predators; it interacts with vector organisms that facilitate dispersal to new habitats, and also with competitors for similar food environments, including competitors from congeneric and also the same species. Full appreciation of this nematode’s biology warrants further exploration of its natural environment and subsequent integration of this information into the well-established laboratory-based research approaches.

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“…The IJ dispersal stage of parasitic nematodes is similar to dauer in several ways: Both are nonfeeding stages with a resistant cuticle (67), and both recognize and exploit carriers/hosts similarly (18,68). One gene class that has been shown to affect dauers and IJs is the neuropeptide-encoding set of genes (27,48).…”

Section: Peptidergic Signaling Downstream Of Sbt-1 Promotes Dauer Entmentioning

confidence: 99%

FMRFamide-like peptides expand the behavioral repertoire of a densely connected nervous system

Lee

Shih

Schaedel

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Animals, including humans, can adapt to environmental stress through phenotypic plasticity. The free-living nematode can adapt to harsh environments by undergoing a whole-animal change, involving exiting reproductive development and entering the stress-resistant dauer larval stage. The dauer is a dispersal stage with dauer-specific behaviors for finding and stowing onto carrier animals, but how dauers acquire these behaviors, despite having a physically limited nervous system of 302 neurons, is poorly understood. We compared dauer and reproductive development using whole-animal RNA sequencing at fine time points and at sufficient depth to measure transcriptional changes within single cells. We detected 8,042 genes differentially expressed during dauer and reproductive development and observed striking up-regulation of neuropeptide genes during dauer entry. We knocked down neuropeptide processing using mutants and demonstrate that neuropeptide signaling promotes the decision to enter dauer rather than reproductive development. We also demonstrate that during dauer neuropeptides modulate the dauer-specific nictation behavior (carrier animal-hitchhiking) and are necessary for switching from repulsion to CO (a carrier animal cue) in nondauers to CO attraction in dauers. We tested individual neuropeptides using CRISPR knockouts and existing strains and demonstrate that the combined effects of and mimic the effects of on nictation and CO attraction. Through meta-analysis, we discovered similar up-regulation of neuropeptides in the dauer-like infective juveniles of diverse parasitic nematodes, suggesting the antiparasitic target potential of SBT-1. Our findings reveal that, under stress, increased neuropeptide signaling in enhances their decision-making accuracy and expands their behavioral repertoire.

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Host orientation using volatiles in the phoretic nematode Caenorhabditis japonica

Cited by 12 publications

References 24 publications

Transcriptional variation and divergence of host-finding behaviour in Steinernema carpocapsae infective juveniles

Transcriptional variation and divergence of host-finding behaviour in Steinernema carpocapsae infective juveniles

The Natural Biotic Environment ofCaenorhabditis elegans

FMRFamide-like peptides expand the behavioral repertoire of a densely connected nervous system

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