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

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.

The Effect of Secondary Metabolites Produced by Serratia marcescens on Aedes aegypti and Its Microbiota

“…Indeed, colonization resistance assays using gnotobiotic mosquitoes (i.e., mosquitoes with a known initial microbiota composition) showed that the initial microbiota impacts the colonization efficiency of other S. marcescens strains in Ae. aegypti ( Kozlova et al, 2020 ).…”

The microbiome and mosquito vectorial capacity: rich potential for discovery and translation

“…In contrast, the infection of mosquitoes with the pathogenic fungus Beauveria bassiana causes microbiome dysbiosis and over-proliferation and translocation of Serratia marcescens from the gut to the hemocoel, eventually killing the insect [134]. Microbes can benefit from each other, like symbiotic bacteria and yeast in Drosophila [135], but they can also exclude one another, like Enterobacteriaceae and Serratia [136] or Asaia and Wolbachia [137] in mosquitoes. In flies and mosquitoes, microbiota interactions with Wolbachia occur but these do not influence the ability of Wolbachia to block pathogens [138,139].…”

“…Feeding behaviour is disrupted in Ae. aegypti by Serratia [ 136 ] and in Anopheles mosquitoes when exposed to heat-killed E. coli [ 154 ] or Chromobacterium [ 155 ]. Microbiota also have the potential to affect host-seeking behaviour through modulation of their chemosensory system.…”

The Axenic and Gnotobiotic Mosquito: Emerging Models for Microbiome Host Interactions

“…The genome of S. marcescens encodes several genes for heme uptake and storage, as well as demonstrating alpha-hemolytic activity, i.e., the complete lysis of blood cells ( Chen et al, 2017 ). Yet, fewer females infected with S. marcescens took blood meals in comparison with their uninfected cohorts ( Kozlova et al, 2021 ).…”