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Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts

BACKGROUND: Efficient deconstruction of lignocellulosic biomass into simple sugars in an economically viable manner is a prerequisite for its global acceptance as a feedstock in bioethanol production. This is achieved in nature by suites of enzymes with the capability of efficiently depolymerizing a...

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Autores principales: Singh, Rahul, Bennett, Joseph P., Gupta, Mayank, Sharma, Medha, Eqbal, Danish, Alessi, Anna M., Dowle, Adam A., McQueen-Mason, Simon J., Bruce, Neil C., Yazdani, Syed Shams
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6839054/
https://www.ncbi.nlm.nih.gov/pubmed/31719844
http://dx.doi.org/10.1186/s13068-019-1603-8
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author Singh, Rahul
Bennett, Joseph P.
Gupta, Mayank
Sharma, Medha
Eqbal, Danish
Alessi, Anna M.
Dowle, Adam A.
McQueen-Mason, Simon J.
Bruce, Neil C.
Yazdani, Syed Shams
author_facet Singh, Rahul
Bennett, Joseph P.
Gupta, Mayank
Sharma, Medha
Eqbal, Danish
Alessi, Anna M.
Dowle, Adam A.
McQueen-Mason, Simon J.
Bruce, Neil C.
Yazdani, Syed Shams
author_sort Singh, Rahul
collection PubMed
description BACKGROUND: Efficient deconstruction of lignocellulosic biomass into simple sugars in an economically viable manner is a prerequisite for its global acceptance as a feedstock in bioethanol production. This is achieved in nature by suites of enzymes with the capability of efficiently depolymerizing all the components of lignocellulose. Here, we provide detailed insight into the repertoire of enzymes produced by microorganisms enriched from the gut of the crop pathogen rice yellow stem borer (Scirpophaga incertulas). RESULTS: A microbial community was enriched from the gut of the rice yellow stem borer for enhanced rice straw degradation by sub-culturing every 10 days, for 1 year, in minimal medium with rice straw as the main carbon source. The enriched culture demonstrated high cellulolytic and xylanolytic activity in the culture supernatant. Metatranscriptomic and metaexoproteomic analysis revealed a large array of enzymes potentially involved in rice straw deconstruction. The consortium was found to encode genes ascribed to all five classes of carbohydrate-active enzymes (GHs, GTs, CEs, PLs, and AAs), including carbohydrate-binding modules (CBMs), categorized in the carbohydrate-active enzymes (CAZy) database. The GHs were the most abundant class of CAZymes. Predicted enzymes from these CAZy classes have the potential to digest each cell-wall components of rice straw, i.e., cellulose, hemicellulose, pectin, callose, and lignin. Several identified CAZy proteins appeared novel, having an unknown or hypothetical catalytic counterpart with a known class of CBM. To validate the findings, one of the identified enzymes that belong to the GH10 family was functionally characterized. The enzyme expressed in E. coli efficiently hydrolyzed beechwood xylan, and pretreated and untreated rice straw. CONCLUSIONS: This is the first report describing the enrichment of lignocellulose degrading bacteria from the gut of the rice yellow stem borer to deconstruct rice straw, identifying a plethora of enzymes secreted by the microbial community when growing on rice straw as a carbon source. These enzymes could be important candidates for biorefineries to overcome the current bottlenecks in biomass processing.
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spelling pubmed-68390542019-11-12 Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts Singh, Rahul Bennett, Joseph P. Gupta, Mayank Sharma, Medha Eqbal, Danish Alessi, Anna M. Dowle, Adam A. McQueen-Mason, Simon J. Bruce, Neil C. Yazdani, Syed Shams Biotechnol Biofuels Research BACKGROUND: Efficient deconstruction of lignocellulosic biomass into simple sugars in an economically viable manner is a prerequisite for its global acceptance as a feedstock in bioethanol production. This is achieved in nature by suites of enzymes with the capability of efficiently depolymerizing all the components of lignocellulose. Here, we provide detailed insight into the repertoire of enzymes produced by microorganisms enriched from the gut of the crop pathogen rice yellow stem borer (Scirpophaga incertulas). RESULTS: A microbial community was enriched from the gut of the rice yellow stem borer for enhanced rice straw degradation by sub-culturing every 10 days, for 1 year, in minimal medium with rice straw as the main carbon source. The enriched culture demonstrated high cellulolytic and xylanolytic activity in the culture supernatant. Metatranscriptomic and metaexoproteomic analysis revealed a large array of enzymes potentially involved in rice straw deconstruction. The consortium was found to encode genes ascribed to all five classes of carbohydrate-active enzymes (GHs, GTs, CEs, PLs, and AAs), including carbohydrate-binding modules (CBMs), categorized in the carbohydrate-active enzymes (CAZy) database. The GHs were the most abundant class of CAZymes. Predicted enzymes from these CAZy classes have the potential to digest each cell-wall components of rice straw, i.e., cellulose, hemicellulose, pectin, callose, and lignin. Several identified CAZy proteins appeared novel, having an unknown or hypothetical catalytic counterpart with a known class of CBM. To validate the findings, one of the identified enzymes that belong to the GH10 family was functionally characterized. The enzyme expressed in E. coli efficiently hydrolyzed beechwood xylan, and pretreated and untreated rice straw. CONCLUSIONS: This is the first report describing the enrichment of lignocellulose degrading bacteria from the gut of the rice yellow stem borer to deconstruct rice straw, identifying a plethora of enzymes secreted by the microbial community when growing on rice straw as a carbon source. These enzymes could be important candidates for biorefineries to overcome the current bottlenecks in biomass processing. BioMed Central 2019-11-08 /pmc/articles/PMC6839054/ /pubmed/31719844 http://dx.doi.org/10.1186/s13068-019-1603-8 Text en © The Author(s) 2019 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
Singh, Rahul
Bennett, Joseph P.
Gupta, Mayank
Sharma, Medha
Eqbal, Danish
Alessi, Anna M.
Dowle, Adam A.
McQueen-Mason, Simon J.
Bruce, Neil C.
Yazdani, Syed Shams
Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
title Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
title_full Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
title_fullStr Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
title_full_unstemmed Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
title_short Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
title_sort mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6839054/
https://www.ncbi.nlm.nih.gov/pubmed/31719844
http://dx.doi.org/10.1186/s13068-019-1603-8
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