Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts

Abstract 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 depolyme...

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Main Authors: Rahul Singh, Joseph P. Bennett, Mayank Gupta, Medha Sharma, Danish Eqbal, Anna M. Alessi, Adam A. Dowle, Simon J. McQueen-Mason, Neil C. Bruce, Syed Shams Yazdani
Format: Article
Language:English
Published: BMC 2019-11-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13068-019-1603-8
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spelling doaj-457d18cbbef44d3c94c59f7912a9d9f42020-11-25T04:03:31ZengBMCBiotechnology for Biofuels1754-68342019-11-0112111910.1186/s13068-019-1603-8Mining the biomass deconstructing capabilities of rice yellow stem borer symbiontsRahul Singh0Joseph P. Bennett1Mayank Gupta2Medha Sharma3Danish Eqbal4Anna M. Alessi5Adam A. Dowle6Simon J. McQueen-Mason7Neil C. Bruce8Syed Shams Yazdani9Microbial Engineering Group, International Centre for Genetic Engineering and BiotechnologyDepartment of Biology, Centre for Novel Agricultural Products, University of YorkMicrobial Engineering Group, International Centre for Genetic Engineering and BiotechnologyMicrobial Engineering Group, International Centre for Genetic Engineering and BiotechnologyMicrobial Engineering Group, International Centre for Genetic Engineering and BiotechnologyDepartment of Biology, Centre for Novel Agricultural Products, University of YorkDepartment of Biology, Bioscience Technology Facility, University of YorkDepartment of Biology, Centre for Novel Agricultural Products, University of YorkDepartment of Biology, Centre for Novel Agricultural Products, University of YorkMicrobial Engineering Group, International Centre for Genetic Engineering and BiotechnologyAbstract 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.http://link.springer.com/article/10.1186/s13068-019-1603-8Rice yellow stem borerGut consortiumMicrobial diversityTargeted enrichmentMetaexoproteomeCarbohydrate-active enzymes
collection DOAJ
language English
format Article
sources DOAJ
author Rahul Singh
Joseph P. Bennett
Mayank Gupta
Medha Sharma
Danish Eqbal
Anna M. Alessi
Adam A. Dowle
Simon J. McQueen-Mason
Neil C. Bruce
Syed Shams Yazdani
spellingShingle Rahul Singh
Joseph P. Bennett
Mayank Gupta
Medha Sharma
Danish Eqbal
Anna M. Alessi
Adam A. Dowle
Simon J. McQueen-Mason
Neil C. Bruce
Syed Shams Yazdani
Mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
Biotechnology for Biofuels
Rice yellow stem borer
Gut consortium
Microbial diversity
Targeted enrichment
Metaexoproteome
Carbohydrate-active enzymes
author_facet Rahul Singh
Joseph P. Bennett
Mayank Gupta
Medha Sharma
Danish Eqbal
Anna M. Alessi
Adam A. Dowle
Simon J. McQueen-Mason
Neil C. Bruce
Syed Shams Yazdani
author_sort Rahul Singh
title 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_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_sort mining the biomass deconstructing capabilities of rice yellow stem borer symbionts
publisher BMC
series Biotechnology for Biofuels
issn 1754-6834
publishDate 2019-11-01
description Abstract 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.
topic Rice yellow stem borer
Gut consortium
Microbial diversity
Targeted enrichment
Metaexoproteome
Carbohydrate-active enzymes
url http://link.springer.com/article/10.1186/s13068-019-1603-8
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