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Cultivation of Heligmosomoides Polygyrus: An Immunomodulatory Nematode Parasite and its Secreted Products
Published on: April 6, 2015
Experience-dependent olfactory behaviors of the parasitic nematode Heligmosomoides polygyrus
Felicitas Ruiz1, Michelle L Castelletto1, Spencer S Gang2
1Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, California, United States of America.
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 (CO2) 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.
Insights
Passively ingested parasitic nematodes actively seek hosts using smell, not just waiting to be eaten. Their olfactory responses are flexible and change with experience, offering new ways to prevent parasitic infections.
Area of Science:
- Zoology
- Parasitology
- Neuroethology
Background:
- Parasitic nematodes cause significant global disease and economic losses.
- Many nematodes infect hosts as third-stage larvae (iL3s), with varied infection routes (skin penetration vs. passive ingestion).
- The olfactory behavior of passively ingested iL3s was largely unknown, contrasting with actively host-seeking iL3s.
Purpose of the Study:
- To investigate the olfactory behaviors of passively ingested Heligmosomoides polygyrus iL3s.
- To determine if H. polygyrus iL3s actively navigate toward hosts or new fecal sources.
- To explore the plasticity and experience-dependent modulation of nematode olfactory responses.
Main Methods:
- Behavioral assays examining H. polygyrus iL3 responses to host feces and olfactory cues.
- Observation of iL3 migration patterns from fecal sources.
- Comparative analysis of olfactory plasticity in H. polygyrus and Haemonchus contortus.
Main Results:
- H. polygyrus iL3s exhibit strong attraction to host feces and mammalian skin odorants.
- iL3s actively migrate off feces, demonstrating environmental navigation.
- Olfactory preferences are flexible and experience-dependent, modulated by CO2 levels over days.
- Similar plasticity was observed in the ruminant parasite H. contortus.
Conclusions:
- Passively ingested nematodes actively navigate using olfactory cues, rather than passively waiting for ingestion.
- Olfactory plasticity allows iL3s to switch between dispersal and host-seeking behaviors.
- Understanding and disrupting these sensory-driven behaviors presents a novel strategy for preventing parasitic nematode infections.
