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Experience-dependent olfactory behaviors of the parasitic nematode Heligmosomoides polygyrus

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      Abstract

      Parasitic nematodes of humans and livestock cause extensive disease and economic loss worldwide. Many parasitic nematodes infect hosts as third-stage larvae, called iL3s. iL3s vary in their infection route: some infect by skin penetration, others by passive ingestion. Skin-penetrating iL3s actively search for hosts using host-emitted olfactory cues, but the extent to which passively ingested iL3s respond to olfactory cues was largely unknown. Here, we examined the olfactory behaviors of the passively ingested murine gastrointestinal parasite Heligmosomoides polygyrus. H. polygyrus iL3s were thought to reside primarily on mouse feces, and infect when mice consume feces containing iL3s. However, iL3s can also adhere to mouse fur and infect orally during grooming. Here, we show that H. polygyrus iL3s are highly active and show robust attraction to host feces. Despite their attraction to feces, many iL3s migrate off feces to engage in environmental navigation. In addition, H. polygyrus iL3s are attracted to mammalian skin odorants, suggesting that they migrate toward hosts. The olfactory preferences of H. polygyrus are flexible: some odorants are repulsive for iL3s maintained on feces but attractive for iL3s maintained off feces. Experience-dependent modulation of olfactory behavior occurs over the course of days and is mediated by environmental carbon dioxide (CO 2) levels. Similar experience-dependent olfactory plasticity occurs in the passively ingested ruminant-parasitic nematode Haemonchus contortus, a major veterinary parasite. Our results suggest that passively ingested iL3s migrate off their original fecal source and actively navigate toward hosts or new host fecal sources using olfactory cues. Olfactory plasticity may be a mechanism that enables iL3s to switch from dispersal behavior to host-seeking behavior. Together, our results demonstrate that passively ingested nematodes do not remain inactive waiting to be swallowed, but rather display complex sensory-driven behaviors to position themselves for host ingestion. Disrupting these behaviors may be a new avenue for preventing infections.

      Author summary

      Many parasitic nematodes infect by passive ingestion when the host consumes food, water, or feces containing infective third-stage larvae (iL3s). Passively ingested nematodes that infect humans cause severe gastrointestinal distress and death in endemic regions, and those that infect livestock are a major cause of production loss worldwide. Because these parasites do not actively invade hosts but instead rely on being swallowed by hosts, it has been assumed that they show only limited sensory responses and do not engage in host-seeking behaviors. Here, we investigate the olfactory behaviors of the passively ingested murine parasite Heligmosomoides polygyrus and show that this assumption is incorrect; H. polygyrus iL3s show robust attraction to a diverse array of odorants found in mammalian skin, sweat, and feces. Moreover, the olfactory responses of H. polygyrus iL3s are experience-dependent: some odorants are repulsive to iL3s cultured on feces but attractive to iL3s removed from feces. Olfactory plasticity is also observed in the ruminant parasite Haemonchus contortus, and may enable iL3s to disperse in search of new hosts or host fecal sources. Our results suggest that passively ingested nematodes use olfactory cues to navigate their environments and position themselves where they are likely to be swallowed. By providing new insights into the olfactory behaviors of these parasites, our results may enable the development of new strategies for preventing infections.

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      Most cited references 67

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      Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis.

      More than a quarter of the human population is likely infected with soil-transmitted helminths (Ascaris lumbricoides, hookworm, and Trichuris trichiura) in highly endemic areas. Preventive chemotherapy is the mainstay of control, but only 4 drugs are available: albendazole, mebendazole, levamisole, and pyrantel pamoate. To assess the efficacy of single-dose oral albendazole, mebendazole, levamisole, and pyrantel pamoate against A lumbricoides, hookworm, and T trichiura infections. A systematic search of PubMed, ISI Web of Science, ScienceDirect, the World Health Organization library database, and the Cochrane Central Register of Controlled Trials (1960 to August 2007). From 168 studies, 20 randomized controlled trials were included. Information on study year and country, sample size, age of study population, mean infection intensity before treatment, diagnostic method used, time between evaluations before and after treatment, cure rate (the percentage of individuals who became helminth egg negative following treatment with an anthelminthic drug), egg reduction rate, adverse events, and trial quality was extracted. Relative risk, including a 95% confidence interval (CI), was used to measure the effect of the drugs on the risk of infection prevalence with a random-effects model. Single-dose oral albendazole, mebendazole, and pyrantel pamoate for infection with A lumbricoides resulted in cure rates of 88% (95% CI, 79%-93%; 557 patients), 95% (95% CI, 91%-97%; 309 patients), and 88% (95% CI, 79%-93%; 131 patients), respectively. Cure rates for infection with T trichiura following treatment with single-dose oral albendazole and mebendazole were 28% (95% CI, 13%-39%; 735 patients) and 36% (95% CI, 16%-51%; 685 patients), respectively. The efficacy of single-dose oral albendazole, mebendazole, and pyrantel pamoate against hookworm infections was 72% (95% CI, 59%-81%; 742 patients), 15% (95% CI, 1%-27%; 853 patients), and 31% (95% CI, 19%-42%; 152 patients), respectively. No pooled relative risks could be calculated for pyrantel pamoate against T trichiura and levamisole for any of the parasites investigated. Single-dose oral albendazole, mebendazole, and pyrantel pamoate show high cure rates against A lumbricoides. For hookworm infection, albendazole was more efficacious than mebendazole and pyrantel pamoate. Treatment of T trichiura with single oral doses of current anthelminthics is unsatisfactory. New anthelminthics are urgently needed.
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        Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans.

        The functions of the 11 classes of exposed chemosensory neurons of C. elegans were tested by killing cells with a laser microbeam. One pair of neurons, the ASE neurons, is uniquely important for chemotaxis: killing the ASE neurons greatly reduced chemotaxis to cAMP, biotin, Cl-, and Na+. Additional chemosensory function is distributed among several other cell types. Thus, 3 pairs of chemosensory neurons (ADF, ASG, and ASI) contribute to a residual response to cAMP, biotin, Cl-, and Na+ after ASE is killed. Chemotaxis to lysine similarly depends on the partly redundant functions of 4 pairs of chemosensory neurons (ASE, ASG, ASI, and ASK). The combined activity of several neuron types that act in parallel might increase the fidelity of chemotaxis.
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          The Parallel Worm Tracker: A Platform for Measuring Average Speed and Drug-Induced Paralysis in Nematodes

          Background Caenorhabditis elegans locomotion is a simple behavior that has been widely used to dissect genetic components of behavior, synaptic transmission, and muscle function. Many of the paradigms that have been created to study C. elegans locomotion rely on qualitative experimenter observation. Here we report the implementation of an automated tracking system developed to quantify the locomotion of multiple individual worms in parallel. Methodology/Principal Findings Our tracking system generates a consistent measurement of locomotion that allows direct comparison of results across experiments and experimenters and provides a standard method to share data between laboratories. The tracker utilizes a video camera attached to a zoom lens and a software package implemented in MATLAB®. We demonstrate several proof-of-principle applications for the tracker including measuring speed in the absence and presence of food and in the presence of serotonin. We further use the tracker to automatically quantify the time course of paralysis of worms exposed to aldicarb and levamisole and show that tracker performance compares favorably to data generated using a hand-scored metric. Conclusions/Signficance Although this is not the first automated tracking system developed to measure C. elegans locomotion, our tracking software package is freely available and provides a simple interface that includes tools for rapid data collection and analysis. By contrast with other tools, it is not dependent on a specific set of hardware. We propose that the tracker may be used for a broad range of additional worm locomotion applications including genetic and chemical screening.
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            Author and article information

            Affiliations
            [1 ] Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, California, United States of America
            [2 ] Molecular Biology Institute, University of California, Los Angeles, Los Angeles, California, United States of America
            University of Glasgow, UNITED KINGDOM
            Author notes

            The authors have declared that no competing interests exist.

            Contributors
            ORCID: http://orcid.org/0000-0003-4596-5247, Role: Conceptualization, Role: Investigation, Role: Methodology, Role: Writing – original draft, Role: Writing – review & editing
            Role: Investigation, Role: Methodology, Role: Writing – review & editing
            Role: Investigation, Role: Methodology, Role: Writing – review & editing
            ORCID: http://orcid.org/0000-0003-0260-3174, Role: Conceptualization, Role: Formal analysis, Role: Funding acquisition, Role: Methodology, Role: Project administration, Role: Supervision, Role: Writing – original draft, Role: Writing – review & editing
            Role: Editor
            Journal
            PLoS Pathog
            PLoS Pathog
            plos
            plospath
            PLoS Pathogens
            Public Library of Science (San Francisco, CA USA )
            1553-7366
            1553-7374
            30 November 2017
            November 2017
            : 13
            : 11
            29190282
            5708605
            10.1371/journal.ppat.1006709
            PPATHOGENS-D-17-00258
            (Editor)
            © 2017 Ruiz et al

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

            Counts
            Figures: 7, Tables: 0, Pages: 23
            Product
            Funding
            Funded by: funder-id http://dx.doi.org/10.13039/100000052, NIH Office of the Director;
            Award ID: 1DP2DC014596
            Award Recipient : ORCID: http://orcid.org/0000-0003-0260-3174
            This work was supported by a National Institutes of Health New Innovator Award (1DP2DC014596) to EAH. FR is a UCLA Center for Academic & Research Excellence (CARE) Scholar, and was supported by National Institute of General Medical Sciences grant R25GM055052 to T. Hasson. SSG was supported by a Microbial Pathogenesis Training Grant from the National Institute of Allergy and Infectious Diseases (AI007323). EAH is a MacArthur Fellow and Howard Hughes Medical Institute Faculty Scholar. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Categories
            Research Article
            Earth Sciences
            Atmospheric Science
            Atmospheric Chemistry
            Greenhouse Gases
            Carbon Dioxide
            Physical Sciences
            Chemistry
            Environmental Chemistry
            Atmospheric Chemistry
            Greenhouse Gases
            Carbon Dioxide
            Ecology and Environmental Sciences
            Environmental Chemistry
            Atmospheric Chemistry
            Greenhouse Gases
            Carbon Dioxide
            Physical Sciences
            Chemistry
            Chemical Compounds
            Carbon Dioxide
            Medicine and Health Sciences
            Parasitic Diseases
            Nematode Infections
            Physical Sciences
            Materials Science
            Materials by Attribute
            Odorants
            Medicine and Health Sciences
            Parasitic Diseases
            Biology and Life Sciences
            Behavior
            Biology and Life Sciences
            Organisms
            Eukaryota
            Animals
            Invertebrates
            Nematoda
            Strongyloides
            Strongyloides Stercoralis
            Research and Analysis Methods
            Bioassays and Physiological Analysis
            Cell Analysis
            Chemotaxis Assay
            Biology and Life Sciences
            Behavior
            Animal Behavior
            Animal Migration
            Animal Navigation
            Biology and Life Sciences
            Zoology
            Animal Behavior
            Animal Migration
            Animal Navigation
            Custom metadata
            All relevant data are within the paper and its Supporting Information files.

            Infectious disease & Microbiology

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