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Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure

BACKGROUND: Higher ratios of syringyl-to-guaiacyl (S/G) lignin components of Populus were shown to improve sugar release by enzymatic hydrolysis using commercial blends. Cellulolytic microbes are often robust biomass hydrolyzers and may offer cost advantages; however, it is unknown whether their act...

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Autores principales: Dumitrache, Alexandru, Akinosho, Hannah, Rodriguez, Miguel, Meng, Xianzhi, Yoo, Chang Geun, Natzke, Jace, Engle, Nancy L., Sykes, Robert W., Tschaplinski, Timothy J., Muchero, Wellington, Ragauskas, Arthur J., Davison, Brian H., Brown, Steven D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4743434/
https://www.ncbi.nlm.nih.gov/pubmed/26855670
http://dx.doi.org/10.1186/s13068-016-0445-x
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author Dumitrache, Alexandru
Akinosho, Hannah
Rodriguez, Miguel
Meng, Xianzhi
Yoo, Chang Geun
Natzke, Jace
Engle, Nancy L.
Sykes, Robert W.
Tschaplinski, Timothy J.
Muchero, Wellington
Ragauskas, Arthur J.
Davison, Brian H.
Brown, Steven D.
author_facet Dumitrache, Alexandru
Akinosho, Hannah
Rodriguez, Miguel
Meng, Xianzhi
Yoo, Chang Geun
Natzke, Jace
Engle, Nancy L.
Sykes, Robert W.
Tschaplinski, Timothy J.
Muchero, Wellington
Ragauskas, Arthur J.
Davison, Brian H.
Brown, Steven D.
author_sort Dumitrache, Alexandru
collection PubMed
description BACKGROUND: Higher ratios of syringyl-to-guaiacyl (S/G) lignin components of Populus were shown to improve sugar release by enzymatic hydrolysis using commercial blends. Cellulolytic microbes are often robust biomass hydrolyzers and may offer cost advantages; however, it is unknown whether their activity can also be significantly influenced by the ratio of different monolignol types in Populus biomass. Hydrolysis and fermentation of autoclaved, but otherwise not pretreated Populus trichocarpa by Clostridium thermocellum ATCC 27405 was compared using feedstocks that had similar carbohydrate and total lignin contents but differed in S/G ratios. RESULTS: Populus with an S/G ratio of 2.1 was converted more rapidly and to a greater extent compared to similar biomass that had a ratio of 1.2. For either microbes or commercial enzymes, an approximate 50 % relative difference in total solids solubilization was measured for both biomasses, which suggests that the differences and limitations in the microbial breakdown of lignocellulose may be largely from the enzymatic hydrolytic process. Surprisingly, the reduction in glucan content per gram solid in the residual microbially processed biomass was similar (17–18 %) irrespective of S/G ratio, pointing to a similar mechanism of solubilization that proceeded at different rates. Fermentation metabolome testing did not reveal the release of known biomass-derived alcohol and aldehyde inhibitors that could explain observed differences in microbial hydrolytic activity. Biomass-derived p-hydroxybenzoic acid was up to nine-fold higher in low S/G ratio biomass fermentations, but was not found to be inhibitory in subsequent test fermentations. Cellulose crystallinity and degree of polymerization did not vary between Populus lines and had minor changes after fermentation. However, lignin molecular weights and cellulose accessibility determined by Simons’ staining were positively correlated to the S/G content. CONCLUSIONS: Higher S/G ratios in Populus biomass lead to longer and more linear lignin chains and greater access to surface cellulosic content by microbe-bound enzymatic complexes. Substrate access limitation is suggested as a primary bottleneck in solubilization of minimally processed Populus, which has important implications for microbial deconstruction of lignocellulose biomass. Our findings will allow others to examine different Populus lines and to test if similar observations are possible for other plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0445-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-47434342016-02-06 Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure Dumitrache, Alexandru Akinosho, Hannah Rodriguez, Miguel Meng, Xianzhi Yoo, Chang Geun Natzke, Jace Engle, Nancy L. Sykes, Robert W. Tschaplinski, Timothy J. Muchero, Wellington Ragauskas, Arthur J. Davison, Brian H. Brown, Steven D. Biotechnol Biofuels Research BACKGROUND: Higher ratios of syringyl-to-guaiacyl (S/G) lignin components of Populus were shown to improve sugar release by enzymatic hydrolysis using commercial blends. Cellulolytic microbes are often robust biomass hydrolyzers and may offer cost advantages; however, it is unknown whether their activity can also be significantly influenced by the ratio of different monolignol types in Populus biomass. Hydrolysis and fermentation of autoclaved, but otherwise not pretreated Populus trichocarpa by Clostridium thermocellum ATCC 27405 was compared using feedstocks that had similar carbohydrate and total lignin contents but differed in S/G ratios. RESULTS: Populus with an S/G ratio of 2.1 was converted more rapidly and to a greater extent compared to similar biomass that had a ratio of 1.2. For either microbes or commercial enzymes, an approximate 50 % relative difference in total solids solubilization was measured for both biomasses, which suggests that the differences and limitations in the microbial breakdown of lignocellulose may be largely from the enzymatic hydrolytic process. Surprisingly, the reduction in glucan content per gram solid in the residual microbially processed biomass was similar (17–18 %) irrespective of S/G ratio, pointing to a similar mechanism of solubilization that proceeded at different rates. Fermentation metabolome testing did not reveal the release of known biomass-derived alcohol and aldehyde inhibitors that could explain observed differences in microbial hydrolytic activity. Biomass-derived p-hydroxybenzoic acid was up to nine-fold higher in low S/G ratio biomass fermentations, but was not found to be inhibitory in subsequent test fermentations. Cellulose crystallinity and degree of polymerization did not vary between Populus lines and had minor changes after fermentation. However, lignin molecular weights and cellulose accessibility determined by Simons’ staining were positively correlated to the S/G content. CONCLUSIONS: Higher S/G ratios in Populus biomass lead to longer and more linear lignin chains and greater access to surface cellulosic content by microbe-bound enzymatic complexes. Substrate access limitation is suggested as a primary bottleneck in solubilization of minimally processed Populus, which has important implications for microbial deconstruction of lignocellulose biomass. Our findings will allow others to examine different Populus lines and to test if similar observations are possible for other plant species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0445-x) contains supplementary material, which is available to authorized users. BioMed Central 2016-02-04 /pmc/articles/PMC4743434/ /pubmed/26855670 http://dx.doi.org/10.1186/s13068-016-0445-x Text en © Dumitrache et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 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.
spellingShingle Research
Dumitrache, Alexandru
Akinosho, Hannah
Rodriguez, Miguel
Meng, Xianzhi
Yoo, Chang Geun
Natzke, Jace
Engle, Nancy L.
Sykes, Robert W.
Tschaplinski, Timothy J.
Muchero, Wellington
Ragauskas, Arthur J.
Davison, Brian H.
Brown, Steven D.
Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
title Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
title_full Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
title_fullStr Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
title_full_unstemmed Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
title_short Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
title_sort consolidated bioprocessing of populus using clostridium (ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4743434/
https://www.ncbi.nlm.nih.gov/pubmed/26855670
http://dx.doi.org/10.1186/s13068-016-0445-x
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