Loss of cilia in chemosensory neurons inhibits pathogen avoidance in Caenorhabditis elegans

• Published in: Microbes and infection 2024-11, Vol.26 (8), p.105370, Article 105370
• Main Authors: Lei, Ming, Tan, Yanheng, Ke, Jingyi, Wang, Mengqi, He, Zeyang, Ou, Guangshuo, Tu, Haijun, Tan, Weihong
• Format: Article
• Language: English
• Subjects: Animals; Caenorhabditis elegans - microbiology; Caenorhabditis elegans Proteins - genetics; Caenorhabditis elegans Proteins - metabolism; Chemoreceptor Cells - metabolism; Chemoreceptor Cells - physiology; Cilia - microbiology; Cilia - physiology; Escherichia coli - genetics; Escherichia coli - physiology; External stimulus; Intestinal colonization; Mutation; Neuronal cilia; Neurons - microbiology; Neurons - physiology; Pathogen avoidance; Pseudomonas aeruginosa; Pseudomonas aeruginosa - physiology; RNA-Sequencing
• ISSN: 1286-4579; 1769-714X; 1769-714X
• DOI: 10.1016/j.micinf.2024.105370

Pathogen avoidance is a crucial and evolutionarily conserved behavior that enhances survival by preventing infection in diverse species, including Caenorhabditis elegans (C. elegans). This behavior relies on multiple chemosensory neurons equipped with cilia that are exposed to the external environment. However, the specific role of neuronal cilia in pathogen avoidance has not been completely elucidated. Herein, we discovered that osm-3(p802) mutants, which lack chemosensory neuronal cilia, exhibit slower avoidance of the pathogen Pseudomonas aeruginosa PA14, but not Escherichia coli OP50. This observation was consistent when osm-3(p802) mutants were exposed to P. aeruginosa PAO1. Following an encounter with PA14, the pumping, thrashing, and defecation behaviors of osm-3 mutants were comparable to those of the wild-type. However, the osm-3 mutants demonstrated reduced intestinal colonization of PA14, suggesting that they have stronger intestinal clearance ability. We conducted RNA-seq to identify genes responding to external stimuli that were differentially expressed owing to the loss of osm-3 and PA14 infection. Using RNAi, we demonstrated that three of these genes were essential for normal pathogen avoidance. In conclusion, our findings demonstrate that the loss of chemosensory neuronal cilia reduces pathogen avoidance in C. elegans while delaying intestinal colonization.