The mosquito microbiota can influence host physiology and vector competence, but a detailed understanding of these processes is lacking. Here we found that the gut microbiota of Anopheles stephensi, a competent malaria vector, is involved in tryptophan metabolism and is responsible for the catabolism of the peritrophic matrix impairing tryptophan metabolites. Antibiotic elimination of the microbiota led to the accumulation of tryptophan and its metabolites-kynurenine, 3-hydroxykynurenine (3-HK) and xanthurenic acid. Of these metabolites, 3-HK impaired the structure of the peritrophic matrix and promoted Plasmodium berghei infection. Among the major gut microbiota members in A.stephensi, Pseudomonas alcaligenes catabolized 3-HK as revealed by whole-genome sequencing and LC-MS metabolic analysis. The genome of P. alcaligenes encodes kynureninase (KynU) that is responsible for the conversion of 3-HK to 3-hydroxyanthranilic acid. Mutation of KynU resulted in a P. alcaligenes strain that was unable to metabolize 3-HK and unable to protect the peritrophic matrix. Colonization of A.stephensi with KynU-mutated P. alcaligenes failed to protect mosquitoes against parasite infection as compared with mosquitoes colonized with wild-type P. alcaligenes. In summary, this study identifies an unexpected function of mosquito gut microbiota in controlling mosquito tryptophan metabolism, with important implications for vector competence. The mosquito gut resident bacterium Pseudomonas alcaligenes protects the integrity of the mosquito peritrophic matrix by catabolizing 3-hydroxykynurenine, thereby contributing to protection against Plasmodium infection.
[1]Fudan Univ, State Key Lab Genet Engn, Key Lab Contemporary Anthropol, Minist Educ,Sch Life Sci, Shanghai, Peoples R China.
[2]Fudan Univ, Metabon & Syst Biol Lab, Shanghai Int Ctr Mol Phen, Human Phenome Inst,Zhongshan Hosp, Shanghai, Peoples R China.
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