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      NMR studies on lignocellulose deconstructions in the digestive system of the lower termite Coptotermes formosanus Shiraki

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          Abstract

          Termites represent one of the most efficient lignocellulose decomposers on earth. The mechanism by which termites overcome the recalcitrant lignin barrier to gain access to embedded polysaccharides for assimilation and energy remains largely unknown. In the present study, softwood, hardwood, and grass lignocellulose diets were fed to Coptotermes formosanus workers, and structural differences between the original lignocellulose diets and the resulting feces were examined by solution-state multidimensional nuclear magnetic resonance (NMR) techniques as well as by complementary wet-chemical methods. Overall, our data support the view that lignin polymers are partially decomposed during their passage through the termite gut digestive system, although polysaccharide decomposition clearly dominates the overall lignocellulose deconstruction process and the majority of lignin polymers remain intact in the digestive residues. High-resolution NMR structural data suggested preferential removal of syringyl aromatic units in hardwood lignins, but non-acylated guaiacyl units as well as tricin end-units in grass lignins. In addition, our data suggest that termites and/or their gut symbionts may favor degradation of C–C-bonded β–5 and resinol-type β–β lignin inter-monomeric units over degradation of ether-bonded β– O–4 units, which is in contrast to what has been observed in typical lignin biodegradation undertaken by wood-decaying fungi.

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          Symbiotic digestion of lignocellulose in termite guts.

          Their ability to degrade lignocellulose gives termites an important place in the carbon cycle. This ability relies on their partnership with a diverse community of bacterial, archaeal and eukaryotic gut symbionts, which break down the plant fibre and ferment the products to acetate and variable amounts of methane, with hydrogen as a central intermediate. In addition, termites rely on the biosynthetic capacities of their gut microbiota as a nutritional resource. The mineralization of humus components in the guts of soil-feeding species also contributes to nitrogen cycling in tropical soils. Lastly, the high efficiency of their minute intestinal bioreactors makes termites promising models for the industrial conversion of lignocellulose into microbial products and the production of biofuels.
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            Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview.

            In nature, cellulose, lignocellulose and lignin are major sources of plant biomass; therefore, their recycling is indispensable for the carbon cycle. Each polymer is degraded by a variety of microorganisms which produce a battery of enzymes that work synergically. In the near future, processes that use lignocellulolytic enzymes or are based on microorganisms could lead to new, environmentally friendly technologies. This study reviews recent advances in the various biological treatments that can turn these three lignicellulose biopolymers into alternative fuels. In addition, biotechnological innovations based on natural delignification and applied to pulp and paper manufacture are also outlined.
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              Opportunities and challenges in biological lignin valorization.

              Lignin is a primary component of lignocellulosic biomass that is an underutilized feedstock in the growing biofuels industry. Despite the fact that lignin depolymerization has long been studied, the intrinsic heterogeneity of lignin typically leads to heterogeneous streams of aromatic compounds, which in turn present significant technical challenges when attempting to produce lignin-derived chemicals where purity is often a concern. In Nature, microorganisms often encounter this same problem during biomass turnover wherein powerful oxidative enzymes produce heterogeneous slates of aromatics compounds. Some microbes have evolved metabolic pathways to convert these aromatic species via 'upper pathways' into central intermediates, which can then be funneled through 'lower pathways' into central carbon metabolism in a process we dubbed 'biological funneling'. This funneling approach offers a direct, biological solution to overcome heterogeneity problems in lignin valorization for the modern biorefinery. Coupled to targeted separations and downstream chemical catalysis, this concept offers the ability to produce a wide range of molecules from lignin. This perspective describes research opportunities and challenges ahead for this new field of research, which holds significant promise towards a biorefinery concept wherein polysaccharides and lignin are treated as equally valuable feedstocks. In particular, we discuss tailoring the lignin substrate for microbial utilization, host selection for biological funneling, ligninolytic enzyme-microbe synergy, metabolic engineering, expanding substrate specificity for biological funneling, and process integration, each of which presents key challenges. Ultimately, for biological solutions to lignin valorization to be viable, multiple questions in each of these areas will need to be addressed, making biological lignin valorization a multidisciplinary, co-design problem.
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                Author and article information

                Contributors
                ytobimatsu@rish.kyoto-u.ac.jp
                tsuyoshi@rish.kyoto-u.ac.jp
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                22 January 2018
                22 January 2018
                2018
                : 8
                : 1290
                Affiliations
                [1 ]ISNI 0000 0004 0372 2033, GRID grid.258799.8, Research Institute for Sustainable Humanosphere (RISH), , Kyoto University, Gokasho Uji, ; Kyoto, 611-0011 Japan
                [2 ]Research Center for Biomaterials, Indonesian Institute of Sciences (LIPI), Jl. Raya Bogor KM.46, Cibinong, Bogor, West Java, 16911 Indonesia
                [3 ]ISNI 0000 0004 0372 2033, GRID grid.258799.8, Research Unit for Development and Global Sustainability, , Kyoto University, Gokasho, Uji, ; Kyoto, 611-0011 Japan
                Author information
                http://orcid.org/0000-0002-7578-7392
                Article
                19562
                10.1038/s41598-018-19562-0
                5778066
                29358744
                1a7b205c-311a-4e71-85d4-cddcd1ce5e34
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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                : 16 November 2017
                : 3 January 2018
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