Plant cell walls represent the most abundant pool of organic carbon in terrestrial ecosystems but are highly recalcitrant to utilization by microbes and herbivores owing to the physical and chemical barrier provided by lignin biopolymers. Termites are a paradigmatic example of an organism's having evolved the ability to substantially degrade lignified woody plants, yet atomic-scale characterization of lignin depolymerization by termites remains elusive. We report that the phylogenetically derived termite Nasutitermes sp. efficiently degrades lignin via substantial depletion of major interunit linkages and methoxyls by combining isotope-labeled feeding experiments and solution-state and solid-state nuclear magnetic resonance spectroscopy. Exploring the evolutionary origin of lignin depolymerization in termites, we reveal that the early-diverging woodroach Cryptocercus darwini has limited capability in degrading lignocellulose, leaving most polysaccharides intact. Conversely, the phylogenetically basal lineages of "lower"termites are able to disrupt the lignin-polysaccharide inter- and intramolecular bonding while leaving lignin largely intact. These findings advance knowledge on the elusive but efficient delignification in natural systems with implications for next-generation ligninolytic agents.
|State||Published - May 2023|
Bibliographical noteFunding Information:
Acknowledgments: W e thank K. Hirth (Forest Products Laboratory) for the GC-MS portion of methoxy analyses and F . Matt (Forest Products Laboratory) for carbohydrate composition and Klason lignin analyses. Funding: This study was funded by the Zhejiang Provincial Natural Science Foundation Project LR21C160001 (to H.L.), and National Natur al Science Foundation of China grant projects 32171796 and 31500528 (to H.L.), 22074070 (to X.K.), 32201319 (to N.L.), and 32071771 (to J.M.). J.R. was funded by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER, DE-SC0018409). Author contributions: Conceptualization: H.L., D.J.Y ., X.K., C.R.C., and J.R. Methodology: H.L., X.K., and D.J.Y . Investiga tion: H.L., D.J.Y ., X.K., C.R.C., J.R., and M.Y . Funding acquisition: H.L., X.K., C.R.C., J.R., J.M., and N.L. Supervision: H.L., D.J.Y ., and X.K. Writing—original draft: H.L., D.J.Y ., J.R., and C.R.C. Writing—review and editing: All authors. Competing interests: The authors declare that they hav e no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials.
© 2023 The Authors.
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