Skin-penetrating nematodes exhibit life-stage-specific interactions with host-associated and environmental bacteria

Ivan N Chavez; Taylor M Brown; Adrien Assié; Astra S Bryant; Buck S Samuel; Elissa A Hallem

doi:10.1186/s12915-021-01153-7

Skin-penetrating nematodes exhibit life-stage-specific interactions with host-associated and environmental bacteria

BMC Biol. 2021 Oct 7;19(1):221. doi: 10.1186/s12915-021-01153-7.

Authors

Ivan N Chavez^#¹, Taylor M Brown^#^{1

2}, Adrien Assié^{3

4}, Astra S Bryant¹, Buck S Samuel^{3

4}, Elissa A Hallem^{5

6}

Affiliations

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 Alkek Center for Metagenomics and Microbiome Research, Baylor College of Medicine, Houston, TX, 77030, USA.
⁴ Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, TX, 77030, USA.
⁵ Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA, 90095, USA. ehallem@ucla.edu.
⁶ Molecular Biology Institute, University of California, Los Angeles, Los Angeles, CA, 90095, USA. ehallem@ucla.edu.

^# Contributed equally.

Abstract

Background: Skin-penetrating nematodes of the genus Strongyloides infect over 600 million people, posing a major global health burden. Their life cycle includes both a parasitic and free-living generation. During the parasitic generation, infective third-stage larvae (iL3s) actively engage in host seeking. During the free-living generation, the nematodes develop and reproduce on host feces. At different points during their life cycle, Strongyloides species encounter a wide variety of host-associated and environmental bacteria. However, the microbiome associated with Strongyloides species, and the behavioral and physiological interactions between Strongyloides species and bacteria, remain unclear.

Results: We first investigated the microbiome of the human parasite Strongyloides stercoralis using 16S-based amplicon sequencing. We found that S. stercoralis free-living adults have an associated microbiome consisting of specific fecal bacteria. We then investigated the behavioral responses of S. stercoralis and the closely related rat parasite Strongyloides ratti to an ecologically diverse panel of bacteria. We found that S. stercoralis and S. ratti showed similar responses to bacteria. The responses of both nematodes to bacteria varied dramatically across life stages: free-living adults were strongly attracted to most of the bacteria tested, while iL3s were attracted specifically to a narrow range of environmental bacteria. The behavioral responses to bacteria were dynamic, consisting of distinct short- and long-term behaviors. Finally, a comparison of the growth and reproduction of S. stercoralis free-living adults on different bacteria revealed that the bacterium Proteus mirabilis inhibits S. stercoralis egg hatching, and thereby greatly decreases parasite viability.

Conclusions: Skin-penetrating nematodes encounter bacteria from various ecological niches throughout their life cycle. Our results demonstrate that bacteria function as key chemosensory cues for directing parasite movement in a life-stage-specific manner. Some bacterial genera may form essential associations with the nematodes, while others are detrimental and serve as a potential source of novel nematicides.

Keywords: Bacteria; Chemosensation; Parasitic nematode; Sensory behavior; Strongyloides.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
Bacteria
Larva
Life Cycle Stages
Nematoda*
Rats
Skin
Strongyloides ratti
Strongyloides stercoralis

Abstract

Publication types

MeSH terms

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