The neural basis of heat seeking in a human-infective parasitic worm
Soil-transmitted parasitic nematodes infect over one billion people and cause devastating morbidity worldwide. Many of these parasites have infective larvae that locate hosts using thermal cues. Here, we identify the thermosensory neurons of the human threadworm Strongyloides stercoralis and show th...
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Published in | Current biology Vol. 32; no. 10; pp. 2206 - 2221.e6 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
23.05.2022
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Abstract | Soil-transmitted parasitic nematodes infect over one billion people and cause devastating morbidity worldwide. Many of these parasites have infective larvae that locate hosts using thermal cues. Here, we identify the thermosensory neurons of the human threadworm Strongyloides stercoralis and show that they display unique functional adaptations that enable the precise encoding of temperatures up to human body temperature. We demonstrate that experience-dependent thermal plasticity regulates the dynamic range of these neurons while preserving their ability to encode host-relevant temperatures. We describe a novel behavior in which infective larvae spontaneously reverse attraction to heat sources at sub-body temperatures and show that this behavior is mediated by rapid adaptation of the thermosensory neurons. Finally, we identify thermoreceptors that confer parasite-specific sensitivity to body heat. Our results pinpoint the parasite-specific neural adaptations that enable parasitic nematodes to target humans and provide the foundation for drug development to prevent human infection.
•S. stercoralis senses temperature via the conserved AFD sensory neuron pair•Heat seeking by S. stercoralis infective larvae requires Ss-AFD neurons•Ss-AFD neurons display unique temperature-encoding strategies•Three receptor-type guanylate cyclases in Ss-AFD sense body heat
Bryant et al. report that the skin-penetrating, human-parasitic nematode Strongyloides stercoralis relies on a conserved thermosensory neuron pair to drive attraction to human body heat. The authors demonstrate that parasite-specific sensory encoding strategies drive temperature-driven host seeking by human-infective parasitic worms. |
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AbstractList | Soil-transmitted parasitic nematodes infect over one billion people and cause devastating morbidity worldwide. Many of these parasites have infective larvae that locate hosts using thermal cues. Here, we identify the thermosensory neurons of the human threadworm Strongyloides stercoralis and show that they display unique functional adaptations that enable the precise encoding of temperatures up to human body temperature. We demonstrate that experience-dependent thermal plasticity regulates the dynamic range of these neurons while preserving their ability to encode host-relevant temperatures. We describe a novel behavior in which infective larvae spontaneously reverse attraction to heat sources at sub-body temperatures and show that this behavior is mediated by rapid adaptation of the thermosensory neurons. Finally, we identify thermoreceptors that confer parasite-specific sensitivity to body heat. Our results pinpoint the parasite-specific neural adaptations that enable parasitic nematodes to target humans and provide the foundation for drug development to prevent human infection. Soil-transmitted parasitic nematodes infect over one billion people and cause devastating morbidity worldwide. Many of these parasites have infective larvae that locate hosts using thermal cues. Here, we identify the thermosensory neurons of the human threadworm Strongyloides stercoralis and show that they display unique functional adaptations that enable the precise encoding of temperatures up to human body temperature. We demonstrate that experience-dependent thermal plasticity regulates the dynamic range of these neurons while preserving their ability to encode host-relevant temperatures. We describe a novel behavior in which infective larvae spontaneously reverse attraction to heat sources at sub-body temperatures and show that this behavior is mediated by rapid adaptation of the thermosensory neurons. Finally, we identify thermoreceptors that confer parasite-specific sensitivity to body heat. Our results pinpoint the parasite-specific neural adaptations that enable parasitic nematodes to target humans and provide the foundation for drug development to prevent human infection. Bryant et al . report that the skin-penetrating, human-parasitic nematode Strongyloides stercoralis relies on a conserved thermosensory neuron pair to drive attraction to human body heat. The authors demonstrate that parasite-specific sensory encoding strategies drive temperature-driven host seeking by human-infective parasitic worms. Soil-transmitted parasitic nematodes infect over one billion people and cause devastating morbidity worldwide. Many of these parasites have infective larvae that locate hosts using thermal cues. Here, we identify the thermosensory neurons of the human threadworm Strongyloides stercoralis and show that they display unique functional adaptations that enable the precise encoding of temperatures up to human body temperature. We demonstrate that experience-dependent thermal plasticity regulates the dynamic range of these neurons while preserving their ability to encode host-relevant temperatures. We describe a novel behavior in which infective larvae spontaneously reverse attraction to heat sources at sub-body temperatures and show that this behavior is mediated by rapid adaptation of the thermosensory neurons. Finally, we identify thermoreceptors that confer parasite-specific sensitivity to body heat. Our results pinpoint the parasite-specific neural adaptations that enable parasitic nematodes to target humans and provide the foundation for drug development to prevent human infection. •S. stercoralis senses temperature via the conserved AFD sensory neuron pair•Heat seeking by S. stercoralis infective larvae requires Ss-AFD neurons•Ss-AFD neurons display unique temperature-encoding strategies•Three receptor-type guanylate cyclases in Ss-AFD sense body heat Bryant et al. report that the skin-penetrating, human-parasitic nematode Strongyloides stercoralis relies on a conserved thermosensory neuron pair to drive attraction to human body heat. The authors demonstrate that parasite-specific sensory encoding strategies drive temperature-driven host seeking by human-infective parasitic worms. |
Author | Lee, Joon Ha Ruiz, Felicitas Hallem, Elissa A. Bryant, Astra S. |
AuthorAffiliation | 2 Molecular Biology Institute, University of California, Los Angeles, Los Angeles, CA 90095 3 Lead contact 1 Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095 |
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Author_xml | – sequence: 1 givenname: Astra S. surname: Bryant fullname: Bryant, Astra S. organization: Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA – sequence: 2 givenname: Felicitas orcidid: 0000-0003-2175-0356 surname: Ruiz fullname: Ruiz, Felicitas organization: Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA – sequence: 3 givenname: Joon Ha orcidid: 0000-0002-7254-829X surname: Lee fullname: Lee, Joon Ha organization: Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA – sequence: 4 givenname: Elissa A. orcidid: 0000-0003-0260-3174 surname: Hallem fullname: Hallem, Elissa A. email: ehallem@ucla.edu organization: Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA |
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Keywords | C. elegans parasitic nematode heat seeking host-seeking Strongyloides stercoralis AFD neuron parasitic helminth thermosensation thermotaxis calcium imaging |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Present address: Yale Interdepartmental Neuroscience Program, Yale University, 260 Whitney Ave, New Haven, CT 06511 Present address: Molecular & Cellular Biology in Seattle Program, Fred Hutchinson Cancer Research Center, 1100 Fairview Ave N, Seattle, WA 98115 A.S.B. and E.A.H. conceived the study and wrote the manuscript. A.S.B., F.R., and J.L. performed all experiments and analyzed the data. All authors read and approved the final manuscript. Author Contributions |
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SubjectTerms | AFD neuron Animals C. elegans Caenorhabditis elegans calcium imaging heat seeking Helminths host-seeking Hot Temperature Humans Larva - physiology Nematoda - physiology parasitic helminth parasitic nematode Strongyloides stercoralis Strongyloides stercoralis - physiology Thermoreceptors thermosensation thermotaxis |
Title | The neural basis of heat seeking in a human-infective parasitic worm |
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