Pathogenic bacteria modulate pheromone response to promote mating

• Published in: Nature (London) Vol. 613; no. 7943; pp. 324 - 331
• Main Authors: Wu, Taihong, Ge, Minghai, Wu, Min, Duan, Fengyun, Liang, Jingting, Chen, Maoting, Gracida, Xicotencatl, Liu, He, Yang, Wenxing, Dar, Abdul Rouf, Li, Chengyin, Butcher, Rebecca A., Saltzman, Arneet L., Zhang, Yun
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 12.01.2023; Nature Publishing Group
• Subjects: 14/19; 38; 38/35; 38/91; 631/378/3917; 631/378/3919; 64/11; Animals; Avoidance; Bacteria; Caenorhabditis elegans - metabolism; Caenorhabditis elegans - microbiology; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - metabolism; Chemoreceptors; E coli; Exposure; Female; Fertilization; Genetic diversity; Glycolipids - metabolism; Hermaphrodites; Hermaphroditic Organisms - physiology; Histamine; Humanities and Social Sciences; Ingestion; Male; Mating; multidisciplinary; Neurons; Pathogens; Pheromones; Pheromones - metabolism; Plasticity; Pseudomonas aeruginosa - pathogenicity; Pseudomonas aeruginosa - physiology; Receptors, Pheromone - metabolism; Reproduction - physiology; Science; Science (multidisciplinary); Self-fertilization; Sensory Receptor Cells - metabolism; Sexual Behavior, Animal; Social behavior; Worms
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-022-05561-9

Pathogens generate ubiquitous selective pressures and host–pathogen interactions alter social behaviours in many animals 1 – 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 dispersal 5 – 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. Infection of Caenorhabditis elegans by Pseudomonas aeruginosa causes an increased pheromone response via the pheromone receptor STR-44 and increases mating with males, a potential mechanism for promoting adaptation in the host.