Inheritance or Recruitment? The Assembly Mechanisms and Functional Dynamics of Microbial Communities in the Life Cycle of a Wood-Feeding Beetle

Microbial partners enhance the metabolic capabilities of insects, enabling their adaptation to diverse ecological niches. Xylophagous insects have larvae that can digest lignocellulose and cope with plant secondary metabolites (PSMs). However, there is little information in terms of microbiome sources, dynamics and species contributions. This limits our understanding of the interaction between xylophagous insects and the microbiome. Monochamus saltuarius (Cerambycidae) is a significant borer of conifers. We used combined qPCR, host genomic and microbiome metagenomic datasets, as well as in vitro validation experiments to study the dynamics of the associated microbiome and its interactions with M. saltuarius. We evaluated microbial metabolic/biosynthetic contributions and validated their related functions. Our findings revealed that insect growth and development altered the quantity and community composition of associated bacteria and fungi. The egg microbiome was particularly susceptible to alteration due to oviposition pits. Bacterial transmission largely persisted between developmental stages, while fungal re-acquisition primarily originated from the external environment. By reconstructing community pathway maps, we identified the cooperative interactions between the insect and its gut microbiome. As larvae transitioned from phloem to xylem feeding, the functional role of the gut microbiome in various pathways was weakened. Remarkably, high-contribution bacterial species largely overlapped across different functional roles, and these species also showed considerable overlap between phloem and xylem feeding periods. Overall, our study highlights the unique interaction between xylophagous insects and their microbiome, which enhances their ability in lignocellulose digestion, PSMs degradation and the acquisition of essential amino acids, as well as vitamins.