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      A comprehensive study of the promoting effect of manganese on white rot fungal treatment for enzymatic hydrolysis of woody and grass lignocellulose

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          Abstract

          Background

          The efficiency of biological systems as an option for pretreating lignocellulosic biomass has to be improved to make the process practical. Fungal treatment with manganese (Mn) addition for improving lignocellulosic biomass fractionation and enzyme accessibility were investigated in this study. The broad-spectrum effect was tested on two different types of feedstocks with three fungal species. Since the physicochemical and structural properties of biomass were the main changes caused by fungal degradation, detailed characterization of biomass structural features was conducted to understand the mechanism of Mn-enhanced biomass saccharification.

          Results

          The glucose yields of fungal-treated poplar and wheat straw increased by 2.97- and 5.71-fold, respectively, after Mn addition. Particularly, over 90% of glucose yield was achieved in Mn-assisted Pleurotus ostreatus-treated wheat straw. A comparison study using pyrolysis gas chromatography mass spectrometry (Py-GC/MS) and two-dimensional 1H– 13C heteronuclear single quantum coherence (2D HSQC) nuclear magnetic resonance (NMR) spectroscopy was conducted to elucidate the role of Mn addition on fungal disruption of the cross-linked structure of whole plant cell wall. The increased C α-oxidized products was consistent with the enhanced cleavage of the major β-O-4 ether linkages in poplar and wheat straw lignin or in the wheat straw lignin–carbohydrate complexes (LCCs), which led to the reduced condensation degree in lignin and decreased lignin content in Mn-assisted fungal-treated biomass. The correlation analysis and principal component analysis (PCA) further demonstrated that Mn addition to fungal treatment enhanced bond cleavage in lignin, especially the β-O-4 ether linkage cleavage played the dominant role in removing the biomass recalcitrance and contributing to the glucose yield enhancement. Meanwhile, enhanced deconstruction of LCCs was important in reducing wheat straw recalcitrance. The findings provided not only mechanistic insights into the Mn-enhanced biomass digestibility by fungus, but also a strategy for improving biological pretreatment efficiency of lignocellulose.

          Conclusion

          The mechanism of enhanced saccharification of biomass by Mn-assisted fungal treatment mainly through C α-oxidative cleavage of β-O-4 ether linkages further led to the decreased condensation degree in lignin, as a result, biomass recalcitrance was significantly reduced by Mn addition.

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          Supplementary Information

          The online version contains supplementary material available at 10.1186/s13068-021-02024-7.

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          Most cited references46

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          Lignin biosynthesis.

          The lignin biosynthetic pathway has been studied for more than a century but has undergone major revisions over the past decade. Significant progress has been made in cloning new genes by genetic and combined bioinformatics and biochemistry approaches. In vitro enzymatic assays and detailed analyses of mutants and transgenic plants altered in the expression of lignin biosynthesis genes have provided a solid basis for redrawing the monolignol biosynthetic pathway, and structural analyses have shown that plant cell walls can tolerate large variations in lignin content and structure. In some cases, the potential value for agriculture of transgenic plants with modified lignin structure has been demonstrated. This review presents a current picture of monolignol biosynthesis, polymerization, and lignin structure.
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            Biological pretreatment of lignocellulosic biomass--An overview.

            Pretreatment is an important step involved in the production of bioethanol from lignocelluosic biomass. Though several pretreatment regimes are available, biological pretreatment seems to be promising being an eco-friendly process and there is no inhibitor generation during the process. In the current scenario there are few limitations in using this strategy for pilot scale process. The first and foremost one is the long incubation time for effective delignification. This can be minimized to an extent by using suitable microbial consortium. There is an urgent need for research and development activities and fine tuning of the process for the development of an economically viable process. This review presents an overview of various aspects of biological pretreatment, enzymes involved in the process, parameters affecting biological pretreatment as well as future perspectives.
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              How does plant cell wall nanoscale architecture correlate with enzymatic digestibility?

              Greater understanding of the mechanisms contributing to chemical and enzymatic solubilization of plant cell walls is critical for enabling cost-effective industrial conversion of cellulosic biomass to biofuels. Here, we report the use of correlative imaging in real time to assess the impact of pretreatment, as well as the resulting nanometer-scale changes in cell wall structure, upon subsequent digestion by two commercially relevant cellulase systems. We demonstrate that the small, noncomplexed fungal cellulases deconstruct cell walls using mechanisms that differ considerably from those of the larger, multienzyme complexes (cellulosomes). Furthermore, high-resolution measurement of the microfibrillar architecture of cell walls suggests that digestion is primarily facilitated by enabling enzyme access to the hydrophobic cellulose face. The data support the conclusion that ideal pretreatments should maximize lignin removal and minimize polysaccharide modification, thereby retaining the essentially native microfibrillar structure.
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                Author and article information

                Contributors
                fuxiao@hust.edu.cn
                zhangjialong@hust.edu.cn
                xiangyu.gu@wsu.edu
                yuhongbo@hust.edu.cn
                chens@wsu.edu
                Journal
                Biotechnol Biofuels
                Biotechnol Biofuels
                Biotechnology for Biofuels
                BioMed Central (London )
                1754-6834
                6 September 2021
                6 September 2021
                2021
                : 14
                : 176
                Affiliations
                [1 ]GRID grid.33199.31, ISNI 0000 0004 0368 7223, Key Laboratory of Molecular Biophysics of MOE, College of Life Science and Technology, , Huazhong University of Science and Technology, ; Wuhan, 430074 China
                [2 ]GRID grid.30064.31, ISNI 0000 0001 2157 6568, Department of Biological Systems Engineering, , Washington State University, ; Pullman, WA 99164 USA
                Author information
                http://orcid.org/0000-0002-7482-7292
                Article
                2024
                10.1186/s13068-021-02024-7
                8420007
                34488855
                88884f48-7219-46db-ad95-f1e6e2c16c1c
                © The Author(s) 2021

                Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 24 May 2021
                : 23 August 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31870083
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2021

                Biotechnology
                mn addition,fungal treatment,enzymatic hydrolysis,delignification,β-o-4 cleavage,principal component analysis

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