Abstract
BackgroundWood-feeding termite, Coptotermes formosanus Shiraki, represents a highly efficient system for biomass deconstruction and utilization. However, the detailed mechanisms of lignin modification and carbohydrate degradation in this system are still largely elusive.ResultsIn order to reveal the inherent mechanisms for efficient biomass degradation, four different organs (salivary glands, foregut, midgut, and hindgut) within a complete digestive system of a lower termite, C. formosanus, were dissected and collected. Comparative transcriptomics was carried out to analyze these organs using high-throughput RNA sequencing. A total of 71,117 unigenes were successfully assembled, and the comparative transcriptome analyses revealed significant differential distributions of GH (glycosyl hydrolase) genes and auxiliary redox enzyme genes in different digestive organs. Among the GH genes in the salivary glands, the most abundant were GH9, GH22, and GH1 genes. The corresponding enzymes may have secreted into the foregut and midgut to initiate the hydrolysis of biomass and to achieve a lignin-carbohydrate co-deconstruction system. As the most diverse GH families, GH7 and GH5 were primarily identified from the symbiotic protists in the hindgut. These enzymes could play a synergistic role with the endogenous enzymes from the host termite for biomass degradation. Moreover, twelve out of fourteen genes coding auxiliary redox enzymes from the host termite origin were induced by the feeding of lignin-rich diets. This indicated that these genes may be involved in lignin component deconstruction with its redox network during biomass pretreatment.ConclusionThese findings demonstrate that the termite digestive system synergized the hydrolysis and redox reactions in a programmatic process, through different parts of its gut system, to achieve a maximized utilization of carbohydrates. The detailed unique mechanisms identified from the termite digestive system may provide new insights for advanced design of future biorefinery.
Highlights
Wood-feeding termite, Coptotermes formosanus Shiraki, represents a highly efficient system for biomass deconstruction and utilization
The wood-feeding termite system of C. formosanus has been proposed as a dual digestive system in biomass degradation processing co-functioned by termite host and its gut symbionts, where termite host was found to be predominant over symbiotic protists in terms of both gene diversity and its transcript abundance when focused on both CAZyme genes and auxiliary redox genes detected with transcriptomics analysis
Twelve genes that encode extracellular secreted redox enzymes showed some rapid responses towards a wood-rich diet feeding, and very likely, these redox enzymes might be crucial for the lignin modification processing
Summary
Wood-feeding termite, Coptotermes formosanus Shiraki, represents a highly efficient system for biomass deconstruction and utilization. The pretreatment process usually demands extreme temperature, pH, and pressure, which will result in high-energy input and capital investment [1] In this regard, the environmentally friendly and costeffective strategies for biomass deconstruction are imminently needed, and as a matter of fact, the mechanisms in natural biomass utilization systems (NBUS) could potentially provide invaluable insights into the design of new biorefinery strategies [2]. Lower wood-feeding termites represent a very efficient biomass degradation system that accomplishes the degradation processing in hours instead of weeks or months in a fungal system [5, 6] This type of wood-feeding termite can selectively modify and decompose the lignin by ~ 25%, yet accomplish a maximized utilization of cellulose at > 90% and various hemicellulose components at ~ 60% in their digestive system [6,7,8]. The termite’s rapid, effective, and ambient environment, deconstruction of biomass, and its efficient mechanism to utilize carbohydrate provided a unique model system for modern biorefinery design [6, 9]
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