Microbial interactions in the mosquito gut determine Serratia colonization and blood-feeding propensity

Kozlova, Elena V.; Hegde, Shivanand; Roundy, Christopher M.; Golovko, George; Saldaña, Miguel A.; Hart, Charles E.; Anderson, Enyia R.; Hornett, Emily A.; Khanipov, Kamil; Popov, Vsevolod L.; Pimenova, Maria; Zhou, Yiyang; Fovanov, Yuriy; Weaver, Scott C.; Routh, Andrew L.; Heinz, Eva; Hughes, Grant L.

Abstract

How microbe–microbe interactions dictate microbial complexity in the mosquito gut is unclear. Previously we found that, Serratia, a gut symbiont that alters vector competence and is being considered for vector control, poorly colonized Aedes aegypti yet was abundant in Culex quinquefasciatus reared under identical conditions. To investigate the incompatibility between Serratia and Ae. aegypti, we characterized two distinct strains of Serratia marcescens from Cx. quinquefasciatus and examined their ability to infect Ae. aegypti. Both Serratia strains poorly infected Ae. aegypti, but when microbiome homeostasis was disrupted, the prevalence and titers of Serratia were similar to the infection in its native host. Examination of multiple genetically diverse Ae. aegypti lines found microbial interference to S. marcescens was commonplace, however, one line of Ae. aegypti was susceptible to infection. Microbiome analysis of resistant and susceptible lines indicated an inverse correlation between Enterobacteriaceae bacteria and Serratia, and experimental co-infections in a gnotobiotic system recapitulated the interference phenotype. Furthermore, we observed an effect on host behavior; Serratia exposure to Ae. aegypti disrupted their feeding behavior, and this phenotype was also reliant on interactions with their native microbiota. Our work highlights the complexity of host–microbe interactions and provides evidence that microbial interactions influence mosquito behavior.

Citation

Kozlova, E. V., Hegde, S., Roundy, C. M., Golovko, G., Saldaña, M. A., Hart, C. E., …Hughes, G. L. (2021). Microbial interactions in the mosquito gut determine Serratia colonization and blood-feeding propensity. ISME Journal, 15(1), 93-108. https://doi.org/10.1038/s41396-020-00763-3

• Journal Article Type: Article
• Online Publication Date: Sep 7, 2020
• Publication Date: 2021-01
• Deposit Date: May 30, 2023
• Journal: The ISME Journal
• Print ISSN: 1751-7362
• Electronic ISSN: 1751-7370
• Publisher: Nature Publishing Group
• Peer Reviewed: Peer Reviewed
• Volume: 15
• Issue: 1
• Pages: 93-108
• DOI: https://doi.org/10.1038/s41396-020-00763-3
• Keywords: Ecology, Evolution, Behavior and Systematics; Microbiology
• Additional Information: Received: 7 May 2020; Revised: 5 August 2020; Accepted: 25 August 2020; First Online: 7 September 2020; : ; : The authors declare that they have no conflict of interest.