Spatial and temporal diversity of Simulium damnosum s.l. gut microbiota and association with Onchocerca volvulus infection in Cameroon

Abstract

Arthropod microbiota plays an important role in host physiology, and there is growing interest in using vector symbionts to modify vector competence and control parasite transmission. This study aims to characterise the blackfly Simulium damnosum s.l. gut microbiota and to explore possible associations with various bio-ecological determinants of the Onchocerca volvulus establishment and the transmission in blackfly. Adult female blackflies were caught in three Cameroonian health districts belonging to different bioecological zones endemic for onchocerciasis. Flies were dissected and qPCR screened for Onchocerca volvulus infection. The diversity of the blackflies gut microbiota was assessed by high-throughput sequencing of the V3-V4 hypervariable region of the bacterial 16S ribosomal RNA. Subsequent metataxo-genomic, multivariate, and association analysis were used to investigate the variables that influence the microbiota diversity.

Transmission index rates ranging from 20.7 to 6.0 % and 6.2to 2.0 % for infection and infectivity rates, respectively, indicate ongoing transmission of onchocerciasis across all surveyed health districts. The identified bacterial taxa were clustered into four phyla, five classes, and 23 genera. The S. damnosum s.l. gut microbiota was dominated by Wolbachia and by Rosenbergiella in Wolbachia-free Simulium. Significant differences were observed in the diversity of S. damnosum s.l. microbiota concerning parity status (P = 0.007), health district of origin (P = 0.001), and the presence of the Onchocerca volvulus. Simulium from the Bafia health district also showed increased bacterial diversity between two consecutive years (P = 0.001). Four bacterial taxa, including Serratia, were associated with the absence of the O. volvulus infection.

These results indicate that S. damnosum s.l. from different onchocerciasis foci in Cameroon, exhibit distinguishable gut microbial compositions which are dynamic over time. Some bacterial species are associated with the O. volvulus infection and could be further investigated as biological target/tool for vector modified-based onchocerciasis control.