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

Le résumé fourni par la source

The arthropod microbiota plays a crucial role in host physiology, from the complementation of certain metabolic pathways to the bioecological adaptation of vectors. This include blackfly (Simulium sl), the vector of Onchocerca volvulus, a parasitic nematode responsible for onchocerciasis (also known as river blindness). As result, there is growing interest in the use of vector symbionts to modify the competence of vectors and control their ability to transmit parasites. The aim of this study was to decipher the gut microbiota of the black fly and its role in the establishment and transmission of Onchocerca volvulus in the black fly. The ultimate aim was to identify potential bacteria to be used as biological tools/targets for vector control and onchocerciasis elimination. An entomological study was carried out in three health districts endemic for onchocerciasis in Cameroon (Bafia, Yabassi and Ndom districts). Adult female black flies were captured, identified on the basis of morphological identification keys, dissected to assess the parity rate and amplified by real-time PCR to detect Onchocerca volvulus infection. The diversity of the Simulium gut microbiota was assessed by high-throughput sequencing of the V3-V4 hypervariable region of the bacterial 16S rRNA. Metataxo-genomic and association analyses were then used to identify the core microbiome and to study the variables influencing microbial diversity. The parity rate was 12.3% and significantly higher in Bafia district. Transmission index rates ranging from 20.7 – 6.0% and 6.2 – 2.0% for infection and infectivity rates, respectively, indicate ongoing transmission of onchocerciasis in all surveyed districts. The identified taxa were clustered into four phyla, five classes and 23 genera. The Simulium gut microbiota was dominated by Wolbachia, which accounted for 78.6% of the relative abundance. Significant differences were observed in the diversity of Simulium microbiota concerning parity status (P = 0.007), district of origin (P = 0.001), and O. volvulus infection status. Simulium from the Bafia district also showed increased diversity between two consecutive years (P = 0.001). Four bacterial taxa, including Serratia, were associated with the absence of the O. volvulus infection in blackflies. This diversity of the simulium microbiome is the highest reported among arthropods of medical importance. The bacteria Serratia and Asia are known to release antiparasitic molecules in certain arthropods (notably tsetse flies) and are thought to play the same role in simulium. These results indicate that Simulium from different onchocerciasis foci have distinct gut microbial compositions that are dynamic over time. However, certain bacteria are constant and induce the absence of infection by Onchocerca volvulus in the black fly. These biomarkers (bacteria preventing the installation/development of the parasite) may be the subject of further study as a biological target/tool for the control of onchocerciasis using modified vectors.

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