The two-component microbial system of the black soldier fly larvae (BSFL) gut: a plastic microbiota in the midgut, but a stable one in the hindgut

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Abstract

Due to their highly polyphagous capacities, black soldier fly ( Hermetia illucens ) larvae (BSFL) are increasingly valued for their ability to convert organic waste into valuable biomass that can be used for a variety of purposes. These remarkable digestive capabilities are highly dependent on an extremely plastic gut microbiota. However, the distribution and functioning of bacterial communities in the various gut compartments - particularly in the hindgut - remain little understood. In this study, we used a metabarcoding approach based on 16S gene sequencing to investigate the effect of three carbohydrate-rich diets with distinct molecular compositions on the functional diversity of the BSFL gut microbiota. Our results showed that the midgut harbors a highly substrate-sensitive microbiota, with a high abundance of Actinomyces spp., regardless of the substrate. A bacterial diversity oriented toward fatty acid biosynthesis pathways is promoted by starch-rich environment, whereas a lignocellulosic substrate fosters a midgut microbiota dominated by Paenibacillus spp. In contrast, the hindgut exhibits a distinctly stable and homogeneous bacterial composition dominated by Dysgonomonas spp. Overall, our results provide clear evidence of a two-compartment microbial system, in which the midgut primarily serves as a substrate-adaptive primary degradation chamber, while the hindgut functions as a stable terminal compartment for the final processing of residual substrates and the recycling of nutrients. These findings contribute to our understanding of the functional diversity of the bacterial microbiota along the BSFL digestive tract, which is a key factor in explaining this insect’s remarkable polyphagous behavior and optimizing its use for industrial purposes.

Importance

By converting various types of organic waste into protein- and lipid-rich larvae, black soldier fly (BSFL) larvae act as a flexible bio-factory driven by their digestive tract. Yet, the functional diversity of the BSFL gut microbiota remains poorly characterized across the compartments of the digestive tract, with the hindgut still a black box. Grasping these aspects is essential to elucidate how this bio-factory functions and to guide the production of larvae tailored to specific industrial needs. By examining how different carbohydrate-rich diets affect this functional diversity, our research provides clear evidence for a two-compartment microbial system: the midgut functioning as a substrate-adaptive primary degradation chamber, and the hindgut functioning as a stable terminal compartment that processes residual substrate and recycles nutrients, with the genus Dysgonomonas acting as a key taxon. Furthermore, our research identifies pivotal bacterial genera (including Actinomyces and Paenibacillus ) supporting BSFL polyphagy under carbohydrate-rich diets.

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