Metabolic synergy and complementarity in the Ips typographus holobiont

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Abstract

Microbial symbiosis plays a central role in shaping ecological and evolutionary processes, driving the adaptation of host organisms to challenging environments. However, the mechanisms underlying functional integration and metabolic cooperation within holobionts remain poorly understood. Current research often emphasizes the taxonomic composition of microbiomes, but the metabolic interactions that sustain these associations are less explored, especially in nutrient-poor ecosystems. This study addresses this knowledge gap by investigating the metabolic interdependencies and associations within the gut microbiome of the European spruce bark beetle ( Ips typographus , ESBB). Using meta-transcriptomic analyses, we reveal the critical contributions of bacterial and fungal symbionts in facilitating host survival. Our findings show that microbial partners compensate for host metabolic deficiencies, with cross-kingdom cooperation enabling the biosynthesis of essential nutrients such as amino acids and vitamins. Furthermore, a division of labor among microbial taxa is evident, with bacteria primarily degrading plant polymers such as xylan and pectin, and fungi specializing in glucan degradation. Functional redundancy in key pathways suggests an adaptive mechanism to ensure nutrient availability under fluctuating microbial community composition. In addition, we identify a previously unappreciated pathway for nitrogen acquisition via bacterial oxidation of inorganic nitrogen. Our findings highlight the ecological importance of metabolic interdependencies in holobionts and their role in the evolutionary success of symbiotic associations. Our results provide a framework for exploring microbial cooperation in nutrient cycling and resource use.

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