Comparative genomics reveals carbohydrate enzymatic fluctuations and herbivorous adaptations in arthropods.

Background: Arthropods represent the largest and most diverse phylum on Earth, playing a pivotal role in the biosphere. One key to their evolutionary success is their ability to feed on plant material. However, their endogenous enzymatic repertoire, which contributes to plant digestion, remains largely unexplored and poorly understood. Results: We analyzed 815 arthropod proteomes and identified a total of 268,171 carbohydrate-active modules. Our findings revealed a strong correlation between enzymatic content and feeding habits, with herbivorous species possessing significantly higher enzyme levels. We identified widespread carbohydrate-active families across the AA, CBM, GH, and GT classes, and observed a progressive increase in taxa-exclusive families in more recent arthropod lineages. Notably, we highlighted the impact of the transition from ametabolous to holometabolous development on carbohydrate metabolism, as well as the ecological adaptations of different species groups. By reconstructing the ancestral enzymatic profiles of arthropods, we identified significant fluctuations in 10 carbohydrate-active families over time. Conclusions: Our analysis advances the understanding of the evolutionary mechanisms utilized by the megadiverse phylum Arthropoda. We emphasize the critical role of herbivory as a selective force shaping enzymatic strategies, particularly those involved in carbohydrate metabolism. The distribution and exclusivity of carbohydrate-active families across different arthropod groups provide insights into their evolutionary trajectories and offer a clearer picture of the metabolic pathways that led their ancestors to their present forms.