Investigating the degradation of wood cell wall polymers in the gut of termites using NMR spectroscopy

Abstract: Lignocellulose is a supramolecular network formed mainly by the complex polymers cellulose, hemicelluloses, and lignin. Among them, lignin is a ubiquitous and heterogeneous plant cell wall polymer derived mainly from hydroxycinnamyl alcohols via combinatorial radical coupling reactions. Unlike cellulose and hemicelluloses, lignin is an aromatic polymer that contains a variety of ether- and carbon-carbon linkages between monomer-derived units. These properties render the cell wall recalcitrant to chemical depolymerization that is an essential but challenging starting point for entire lignocellulosic industries. Biotechnological efforts to unpack and use these carbon-neutral materials for bioenergy and bioproducts require expensive chemical, physical, or biological processes. Despite the vastly stored carbon in plant biomass, ligninolytic capability on the planet has until now only been understood from an extremely limited range of organisms, other than white rot and brown rot fungi. The evolution of biomass deconstruction in insect-microbial systems has created an intriguing parallel to those of wood decay fungi. Lower termites do have the capability to degrade lignin to a certain degree, as is also seen in brown rot fungi; this approach utilizes wood polysaccharides efficiently while leaving most of the lignin polymer intact although they are able to cleave ether linkages in lignin to gain access to the polysaccharides. As the genome of brown rot fungi, like Rhodonia placenta, encodes no ligninolytic peroxidases, yet they are able to truncate the lignin polymer, the question remains: Do lower termites employ ligninolytic peroxidases or a Fenton system in which electrophilic reactive oxygen species like hydroxyl radicals can cleave lignin? The woodroach, Cryptocercus spp., interestingly displays similar losses in lignin units to those seen in the lower termites. In contrast, the extensive amount of lignin degradation in the more derived Termitidae termites is reminiscent of oxidative attack on the lignin polymer by the white-rot fungi, which produced the first ligninolytic peroxidases to gain stored carbon. These efficient and diverse plant biomass-deconstruction strategies in termites all have the potential to inform industrial saccharification and other biotechnological applications.