Reevaluating Symbiotic Digestion in Cockroaches: Unveiling the Hindgut’s Contribution to Digestion in Wood-Feeding Panesthiinae (Blaberidae)

SIMPLE SUMMARY: The remarkable ability of insects to digest wood has long fascinated researchers due to its rarity and complexity. Wood-feeding termites and passalid beetles have been extensively studied as paradigms, unveiling intricate symbiotic interactions involving endogenous enzymes and gut microbiomes. However, the wood-digesting capabilities of panesthiine cockroaches remain vastly unexplored, offering a unique opportunity to gain fresh insights into this unique dietary specialization. In this study, we investigated cellulase and xylanase activity in the crop, midgut, and hindgut lumens of Panesthia angustipennis and Salganea taiwanensis. Utilizing Percoll density gradient centrifugation, we further fractionated the luminal fluid to further elucidate how the activities are partitioned. The crop emerged as a prominent site for fiber digestion, which agrees with previous reports. However, our findings challenge conventional notions, revealing a significant role for the hindgut, which contributes around one-fifth of cellulase and xylanase activity. Particle-associated and potentially bacterial enzymes dominate the hindgut, which is similar to the digestion strategies of certain termites and passalid beetles. Our study sheds light on the remarkable adaptability of wood-feeding insects and provides valuable clues to their evolutionary success on this challenging, nutrient-poor resource. ABSTRACT: Cockroaches of the subfamily Panesthiinae (family Blaberidae) are among the few major groups of insects feeding on decayed wood. Despite having independently evolved the ability to thrive on this recalcitrant and nitrogen-limited resource, they are among the least studied of all wood-feeding insect groups. In the pursuit of unraveling their unique digestive strategies, we explored cellulase and xylanase activity in the crop, midgut, and hindgut lumens of Panesthia angustipennis and Salganea taiwanensis. Employing Percoll density gradient centrifugation, we further fractionated luminal fluid to elucidate how the activities in the gut lumen are further partitioned. Our findings challenge conventional wisdom, underscoring the significant contribution of the hindgut, which accounts for approximately one-fifth of cellulase and xylanase activity. Particle-associated enzymes, potentially of bacterial origin, dominate hindgut digestion, akin to symbiotic strategies observed in select termites and passalid beetles. Our study sheds new light on the digestive prowess of panesthiine cockroaches, providing invaluable insights into the evolution of wood-feeding insects and their remarkable adaptability to challenging, nutrient-poor substrates.