Thermosensory behaviors of the free-living life stages ofStrongyloidesspecies support parasitism in tropical environments
Authors: Gregory Ben T. , Desouky Mariam , Slaughter Jaidyn , Hallem Elissa A. , Bryant Astra S. 
Published: September 2024

Soil-transmitted parasitic nematodes infect over 1 billion people worldwide and are a common source of neglected disease.Strongyloides stercoralisis a potentially fatal skin-penetrating human parasite that is endemic to tropical and subtropical regions around the world. The complex life cycle ofStrongyloidesspecies 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-livingStrongyloidesadults to navigate and survive soil environments are unknown.S. stercoralisinfective larvae display parasite-specific sensory-driven behaviors, including robust attraction to mammalian body heat. In contrast, the free-living model nematodeCaenorhabditis elegansdisplays thermosensory behaviors that guide adult worms to stay within a physiologically permissive range of environmental temperatures. DoS. stercoralisandC. elegansfree-living adults, which experience similar environmental stressors, display common thermal preferences? Here, we characterize the thermosensory behaviors of the free-living adults ofS. stercoralisas well as those of the closely related rat parasite,Strongyloides ratti. We find thatStrongyloidesfree-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-livingStrongyloidesadults, similar to the effect of temperature onC. eleganslifespan. However, we also find that the reproductive potential of the free-living life stage is enhanced at warmer temperatures, particularly forS. 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.

Author Summary

Soil-transmitted parasitic nematodes infect over 1 billion people and are a major source of neglected disease, particularly in the world’s most resource-limited communities. For most parasitic nematode species, reproductive adults exclusively reside within host animals. Species in the genusStrongyloideshave a unique step in their life cycle that features soil-dwelling, non-parasitic adults. Previous studies of the free-living model nematodeCaenorhabditis eleganshave identified temperature as an important factor in ability of free-living nematodes to survive and reproduce in the environment. Our study investigates how the thermosensory behaviors ofStrongyloidesfree-living adults contribute to their survival as well as their role in amplifying the quantity of infective larvae in the soil. We show thatStrongyloidesfree-living adults display broad thermophilic preferences that are highly distinct from those ofC. elegansadults. We also present the first evidence that thermotaxis acts as a robust mechanism for maximizing the infectious capacity ofStrongyloidesspecies located in tropical climates.