Pathogenic bacteria modulate pheromone response to promote mating

Taihong Wu, Minghai Ge, Min Wu, Fengyun Duan, Jingting Liang, Maoting Chen, Xicotencatl Gracida, He Liu, Wenxing Yang, Abdul Rouf Dar, Chengyin Li, Rebecca A. Butcher, Arneet L. Saltzman and Yun Zhang ()
Additional contact information
Taihong Wu: Harvard University
Minghai Ge: Harvard University
Min Wu: Harvard University
Fengyun Duan: Harvard University
Jingting Liang: Harvard University
Maoting Chen: Harvard University
Xicotencatl Gracida: Harvard University
He Liu: Harvard University
Wenxing Yang: Harvard University
Abdul Rouf Dar: University of Florida
Chengyin Li: University of Toronto
Rebecca A. Butcher: University of Florida
Arneet L. Saltzman: University of Toronto
Yun Zhang: Harvard University

Nature, 2023, vol. 613, issue 7943, 324-331

Abstract: Abstract Pathogens generate ubiquitous selective pressures and host–pathogen interactions alter social behaviours in many animals1–4. However, very little is known about the neuronal mechanisms underlying pathogen-induced changes in social behaviour. Here we show that in adult Caenorhabditis elegans hermaphrodites, exposure to a bacterial pathogen (Pseudomonas aeruginosa) modulates sensory responses to pheromones by inducing the expression of the chemoreceptor STR-44 to promote mating. Under standard conditions, C. elegans hermaphrodites avoid a mixture of ascaroside pheromones to facilitate dispersal5–13. We find that exposure to the pathogenic Pseudomonas bacteria enables pheromone responses in AWA sensory neurons, which mediate attractive chemotaxis, to suppress the avoidance. Pathogen exposure induces str-44 expression in AWA neurons, a process regulated by a transcription factor zip-5 that also displays a pathogen-induced increase in expression in AWA. STR-44 acts as a pheromone receptor and its function in AWA neurons is required for pathogen-induced AWA pheromone response and suppression of pheromone avoidance. Furthermore, we show that C. elegans hermaphrodites, which reproduce mainly through self-fertilization, increase the rate of mating with males after pathogen exposure and that this increase requires str-44 in AWA neurons. Thus, our results uncover a causal mechanism for pathogen-induced social behaviour plasticity, which can promote genetic diversity and facilitate adaptation of the host animals.

Date: 2023
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DOI: 10.1038/s41586-022-05561-9

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