Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments.
Soil-transmitted parasitic nematodes infect over 1 billion people worldwide and are a common source of neglected disease. Strongyloides stercoralis is a potentially fatal skin-penetrating human parasite that is endemic to tropical and subtropical regions around the world. The complex life cycle of S...
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Public Library of Science (PLoS)
2024-12-01
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| Series: | PLoS Neglected Tropical Diseases |
| Online Access: | https://doi.org/10.1371/journal.pntd.0012529 |
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| author | Ben T Gregory Mariam Desouky Jaidyn Slaughter Elissa A Hallem Astra S Bryant |
| author_facet | Ben T Gregory Mariam Desouky Jaidyn Slaughter Elissa A Hallem Astra S Bryant |
| author_sort | Ben T Gregory |
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| description | Soil-transmitted parasitic nematodes infect over 1 billion people worldwide and are a common source of neglected disease. Strongyloides stercoralis is a potentially fatal skin-penetrating human parasite that is endemic to tropical and subtropical regions around the world. The complex life cycle of Strongyloides species is unique among human-parasitic nematodes in that it includes a single free-living generation featuring soil-dwelling, bacterivorous adults whose progeny all develop into infective larvae. The sensory behaviors that enable free-living Strongyloides adults to navigate and survive soil environments are unknown. S. stercoralis infective larvae display parasite-specific sensory-driven behaviors, including robust attraction to mammalian body heat. In contrast, the free-living model nematode Caenorhabditis elegans displays thermosensory behaviors that guide adult worms to stay within a physiologically permissive range of environmental temperatures. Do S. stercoralis and C. elegans free-living adults, which experience similar environmental stressors, display common thermal preferences? Here, we characterize the thermosensory behaviors of the free-living adults of S. stercoralis as well as those of the closely related rat parasite, Strongyloides ratti. We find that Strongyloides free-living adults are exclusively attracted to near-tropical temperatures, despite their inability to infect mammalian hosts. We further show that lifespan is shorter at higher temperatures for free-living Strongyloides adults, similar to the effect of temperature on C. elegans lifespan. However, we also find that the reproductive potential of the free-living life stage is enhanced at warmer temperatures, particularly for S. stercoralis. Together, our results reveal a novel role for thermotaxis to maximize the infectious capacity of obligate parasites and provide insight into the biological adaptations that may contribute to their endemicity in tropical climates. |
| format | Article |
| id | doaj-art-fcf8c2a8f3d2435bb3d27083fa31ccec |
| institution | DOAJ |
| issn | 1935-2727 1935-2735 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Neglected Tropical Diseases |
| spelling | doaj-art-fcf8c2a8f3d2435bb3d27083fa31ccec2025-08-20T02:59:18ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352024-12-011812e001252910.1371/journal.pntd.0012529Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments.Ben T GregoryMariam DesoukyJaidyn SlaughterElissa A HallemAstra S BryantSoil-transmitted parasitic nematodes infect over 1 billion people worldwide and are a common source of neglected disease. Strongyloides stercoralis is a potentially fatal skin-penetrating human parasite that is endemic to tropical and subtropical regions around the world. The complex life cycle of Strongyloides species is unique among human-parasitic nematodes in that it includes a single free-living generation featuring soil-dwelling, bacterivorous adults whose progeny all develop into infective larvae. The sensory behaviors that enable free-living Strongyloides adults to navigate and survive soil environments are unknown. S. stercoralis infective larvae display parasite-specific sensory-driven behaviors, including robust attraction to mammalian body heat. In contrast, the free-living model nematode Caenorhabditis elegans displays thermosensory behaviors that guide adult worms to stay within a physiologically permissive range of environmental temperatures. Do S. stercoralis and C. elegans free-living adults, which experience similar environmental stressors, display common thermal preferences? Here, we characterize the thermosensory behaviors of the free-living adults of S. stercoralis as well as those of the closely related rat parasite, Strongyloides ratti. We find that Strongyloides free-living adults are exclusively attracted to near-tropical temperatures, despite their inability to infect mammalian hosts. We further show that lifespan is shorter at higher temperatures for free-living Strongyloides adults, similar to the effect of temperature on C. elegans lifespan. However, we also find that the reproductive potential of the free-living life stage is enhanced at warmer temperatures, particularly for S. stercoralis. Together, our results reveal a novel role for thermotaxis to maximize the infectious capacity of obligate parasites and provide insight into the biological adaptations that may contribute to their endemicity in tropical climates.https://doi.org/10.1371/journal.pntd.0012529 |
| spellingShingle | Ben T Gregory Mariam Desouky Jaidyn Slaughter Elissa A Hallem Astra S Bryant Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments. PLoS Neglected Tropical Diseases |
| title | Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments. |
| title_full | Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments. |
| title_fullStr | Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments. |
| title_full_unstemmed | Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments. |
| title_short | Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments. |
| title_sort | thermosensory behaviors of the free living life stages of strongyloides species support parasitism in tropical environments |
| url | https://doi.org/10.1371/journal.pntd.0012529 |
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