Gut microbiota metagenomics and mediation of phenol degradation in Bactrocera minax (Diptera, Tephritidae).

Abstract

Gut microbiota mediating insect-plant interactions have many manifestations, either by provisioning missing nutrients, or by overcoming plant defensive reactions. However, the mechanism by which gut microbiota empower insects to survive by overcoming a variety of plant secondary metabolites remains largely unknown. Bactrocera minax larvae develop in immature citrus fruits, which present numerous phenolic compounds that challenge the larvae. To explore the role of gut microbes in host use and adaptability, we uncovered the mechanisms of phenol degradation by gut microbes using metagenomic and metatranscriptomic analyses, and verified the degradation ability of isolated and cultured bacteria. Research on this subject can help develop potential strain for the environmental friendly pest management operations. We demonstrated the ability of gut microbes in B. minax larvae to degrade phenols in unripe citrus. After antibiotic treatment, coniferyl alcohol and coumaric aldehyde significantly reduced the survival rate, body length and body weight of the larvae. The metagenomic and metatranscriptomic analyses in B. minax provided evidence for the presence of genes in bacteria and the related pathway involved in phenol degradation. Among them, Enterococcus faecalis and Serratia marcescens, isolated from the gut of B. minax larvae, played critical roles in phenol degradation. Furthermore, supplementation of E. faecalis and S. marcescens in artificial diets containing coniferyl alcohol and coumaric aldehyde increased the survival rate of larvae. In summary, our results provided the first comprehensive analysis of gut bacterial communities by high-throughput sequencing and elucidated the role of bacteria in phenol degradation in B. minax, which shed light on the mechanism underlying specialist insect adaption to host secondary metabolites via gut bacteria. © 2024 Society of Chemical Industry.