Format

Send to

Choose Destination
Curr Biol. 2018 Jul 23;28(14):2338-2347.e6. doi: 10.1016/j.cub.2018.05.063. Epub 2018 Jul 12.

A Critical Role for Thermosensation in Host Seeking by Skin-Penetrating Nematodes.

Author information

1
Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA.
2
Molecular Biology Institute, University of California, Los Angeles, Los Angeles, CA 90095, USA.
3
Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA 90095, USA; Molecular Biology Institute, University of California, Los Angeles, Los Angeles, CA 90095, USA. Electronic address: ehallem@ucla.edu.

Abstract

Skin-penetrating parasitic nematodes infect approximately one billion people worldwide and are a major source of neglected tropical disease [1-6]. Their life cycle includes an infective third-larval (iL3) stage that searches for hosts to infect in a poorly understood process that involves both thermal and olfactory cues. Here, we investigate the temperature-driven behaviors of skin-penetrating iL3s, including the human-parasitic threadworm Strongyloides stercoralis and the human-parasitic hookworm Ancylostoma ceylanicum. We show that human-parasitic iL3s respond robustly to thermal gradients. Like the free-living nematode Caenorhabditis elegans, human-parasitic iL3s show both positive and negative thermotaxis, and the switch between them is regulated by recent cultivation temperature [7]. When engaging in positive thermotaxis, iL3s migrate toward temperatures approximating mammalian body temperature. Exposing iL3s to a new cultivation temperature alters the thermal switch point between positive and negative thermotaxis within hours, similar to the timescale of thermal plasticity in C. elegans [7]. Thermal plasticity in iL3s may enable them to optimize host finding on a diurnal temperature cycle. We show that temperature-driven responses can be dominant in multisensory contexts such that, when thermal drive is strong, iL3s preferentially engage in temperature-driven behaviors despite the presence of an attractive host odorant. Finally, targeted mutagenesis of the S. stercoralis tax-4 homolog abolishes heat seeking, providing the first evidence that parasitic host-seeking behaviors are generated through an adaptation of sensory cascades that drive environmental navigation in C. elegans [7-10]. Together, our results provide insight into the behavioral strategies and molecular mechanisms that allow skin-penetrating nematodes to target humans.

KEYWORDS:

Ancylostoma ceylanicum; Strongyloides stercoralis; heat seeking; host-seeking behavior; parasitic helminths; parasitic nematodes; skin-penetrating nematodes; thermosensation; thermotaxis

PMID:
30017486
PMCID:
PMC6091634
[Available on 2019-07-23]
DOI:
10.1016/j.cub.2018.05.063

Supplemental Content

Full text links

Icon for Elsevier Science
Loading ...
Support Center