Metatranscriptomic analysis of lignocellulolytic microbial communities involved in high-solids decomposition of rice straw

Simmons, Christopher W.; Reddy, Amitha P.; D’haeseleer, Patrik; Khudyakov, Jane; Billis, Konstantinos; Pati, Amrita; Simmons, Blake A.; Singer, Steven W.; Thelen, Michael P.; VanderGheynst, Jean S.

doi:10.1186/s13068-014-0180-0

Title: Metatranscriptomic analysis of lignocellulolytic microbial communities involved in high-solids decomposition of rice straw

Journal Article · Wed Dec 31 00:00:00 EST 2014 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/s13068-014-0180-0· OSTI ID:1257270

Simmons, Christopher W. ^[1]; Reddy, Amitha P. ^[1]; D’haeseleer, Patrik ^[2]; Khudyakov, Jane ^[2]; Billis, Konstantinos ^[3]; Pati, Amrita ^[3]; Simmons, Blake A. ^[4]; Singer, Steven W. ^[5]; Thelen, Michael P. ^[2]; VanderGheynst, Jean S. ^[1]

Joint BioEnergy Institute, Emeryville, CA (United States); Univ. of California, Davis, CA (United States)
Joint BioEnergy Institute, Emeryville, CA (United States); Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Joint Genome Institute, Walnut Creek, CA (United States)
Joint BioEnergy Institute, Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Joint BioEnergy Institute, Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

New lignocellulolytic enzymes are needed that maintain optimal activity under the harsh conditions present during industrial enzymatic deconstruction of biomass, including high temperatures, the absence of free water, and the presence of inhibitors from the biomass. Enriching lignocellulolytic microbial communities under these conditions provides a source of microorganisms that may yield robust lignocellulolytic enzymes tolerant to the extreme conditions needed to improve the throughput and efficiency of biomass enzymatic deconstruction. Identification of promising enzymes from these systems is challenging due to complex substrate-enzyme interactions and requirements to assay for activity. In this study, metatranscriptomes from compost-derived microbial communities enriched on rice straw under thermophilic and mesophilic conditions were sequenced and analyzed to identify lignocellulolytic enzymes overexpressed under thermophilic conditions. To determine differential gene expression across mesophilic and thermophilic treatments, a method was developed which pooled gene expression by functional category, as indicated by Pfam annotations, since microbial communities performing similar tasks are likely to have overlapping functions even if they share no specific genes. Differential expression analysis identified enzymes from glycoside hydrolase family 48, carbohydrate binding module family 2, and carbohydrate binding module family 33 domains as significantly overexpressed in the thermophilic community. Overexpression of these protein families in the thermophilic community resulted from expression of a small number of genes not currently represented in any protein database. Genes in overexpressed protein families were predominantly expressed by a single Actinobacteria genus, Micromonospora. In conclusion, coupling measurements of deconstructive activity with comparative analyses to identify overexpressed enzymes in lignocellulolytic communities provides a targeted approach for discovery of candidate enzymes for more efficient biomass deconstruction. Furthermore, glycoside hydrolase family 48 cellulases and carbohydrate binding module family 33 polysaccharide monooxygenases with carbohydrate binding module family 2 domains may improve saccharification of lignocellulosic biomass under high-temperature and low moisture conditions relevant to industrial biofuel production.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Joint BioEnergy Institute (JBEI), Emeryville, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); UC Office of the President; USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC02-05CH11231; 237496; AC52-07NA27344

OSTI ID:: 1257270

Alternate ID(s):: OSTI ID: 1860859

Report Number(s):: LLNL-JRNL-831202; PII: 180

Journal Information:: Biotechnology for Biofuels, Vol. 7, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 28 works

Citation information provided by
Web of Science

References (36)

Cleavage of cellulose by a CBM33 protein Forsberg, Zarah; Vaaje-Kolstad, Gustav; Westereng, Bjørge Protein Science, Vol. 20, Issue 9 https://doi.org/10.1002/pro.689	journal	August 2011
Rfam: Wikipedia, clans and the "decimal" release Gardner, P. P.; Daub, J.; Tate, J. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq1129	journal	November 2010
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis Cole, J. R.; Wang, Q.; Cardenas, E. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn879	journal	January 2009
The NCBI Taxonomy database Federhen, S. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1178	journal	December 2011
The water footprint of bioenergy Gerbens-Leenes, W.; Hoekstra, A. Y.; van der Meer, T. H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 25 https://doi.org/10.1073/pnas.0812619106	journal	June 2009
Cellulolytic activity of Actinomycetes isolated from termites (Termitidae) gut Pasti, Maria B.; Belli, Maria L. FEMS Microbiology Letters, Vol. 26, Issue 1 https://doi.org/10.1111/j.1574-6968.1985.tb01574.x	journal	January 1985
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
The Critical Moisture Range for Rapid Microbial Decomposition of Rice Straw During Storage Transactions of the ASABE, Vol. 52, Issue 2 https://doi.org/10.13031/2013.26806	journal	January 2009
Differential expression analysis for sequence count data Anders, Simon; Huber, Wolfgang Genome Biology, Vol. 11, Issue 10 https://doi.org/10.1186/gb-2010-11-10-r106	journal	October 2010
Methods for Pretreatment of Lignocellulosic Biomass for Efficient Hydrolysis and Biofuel Production Kumar, Parveen; Barrett, Diane M.; Delwiche, Michael J. Industrial & Engineering Chemistry Research, Vol. 48, Issue 8, p. 3713-3729 https://doi.org/10.1021/ie801542g	journal	April 2009
Evaluation of High Solids Alkaline Pretreatment of Rice Straw Cheng, Yu-Shen; Zheng, Yi; Yu, Chao Wei Applied Biochemistry and Biotechnology, Vol. 162, Issue 6 https://doi.org/10.1007/s12010-010-8958-4	journal	May 2010
Comparative metatranscriptomic signatures of wood and paper feeding in the gut of the termite Reticulitermes flavipes (Isoptera: Rhinotermitidae) : Termite gut metagene expression Raychoudhury, R.; Sen, R.; Cai, Y. Insect Molecular Biology, Vol. 22, Issue 2 https://doi.org/10.1111/imb.12011	journal	January 2013
Comparative Metagenomic and Metatranscriptomic Analysis of Hindgut Paunch Microbiota in Wood- and Dung-Feeding Higher Termites He, Shaomei; Ivanova, Natalia; Kirton, Edward PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061126	journal	April 2013
Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces Takasuka, Taichi E.; Book, Adam J.; Lewin, Gina R. Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep01030	journal	January 2013
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
Cloning, expression and characterization of a Family 48 exocellulase, Cel48A, from Thermobifida fusca: Thermobifida fusca exocellulase Cel48A Irwin, Diana C.; Zhang, Sheng; Wilson, David B. European Journal of Biochemistry, Vol. 267, Issue 16 https://doi.org/10.1046/j.1432-1327.2000.01546.x	journal	August 2000
Strategies for Enhancing the Effectiveness of Metagenomic-based Enzyme Discovery in Lignocellulolytic Microbial Communities DeAngelis, Kristen M.; Gladden, John M.; Allgaier, Martin BioEnergy Research, Vol. 3, Issue 2 https://doi.org/10.1007/s12155-010-9089-z	journal	March 2010
Microbial metatranscriptomics in a permanent marine oxygen minimum zone: OMZ community gene expression Stewart, Frank J.; Ulloa, Osvaldo; DeLong, Edward F. Environmental Microbiology, Vol. 14, Issue 1 https://doi.org/10.1111/j.1462-2920.2010.02400.x	journal	January 2011
Diversity and dynamics of the microbial community on decomposing wheat straw during mushroom compost production Zhang, Xi; Zhong, Yaohua; Yang, Shida Bioresource Technology, Vol. 170 https://doi.org/10.1016/j.biortech.2014.07.093	journal	October 2014
Isolation and screening of potential actinobacteria for rapid composting of rice straw Kausar, H.; Sariah, M.; Mohd Saud, H. Biodegradation, Vol. 22, Issue 2 https://doi.org/10.1007/s10532-010-9407-3	journal	August 2010
Discovery of Microorganisms and Enzymes Involved in High-Solids Decomposition of Rice Straw Using Metagenomic Analyses Reddy, Amitha P.; Simmons, Christopher W.; D’haeseleer, Patrik PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0077985	journal	October 2013
Interplay between Clostridium thermocellum Family 48 and Family 9 Cellulases in Cellulosomal versus Noncellulosomal States Vazana, Y.; Morais, S.; Barak, Y. Applied and Environmental Microbiology, Vol. 76, Issue 10 https://doi.org/10.1128/AEM.00009-10	journal	March 2010
The Pfam protein families database Bateman, Alex; Coin, Lachlan; Durbin, Richard Nucleic Acids Research, Vol. 32, Issue S1, p. D138-D141 https://doi.org/10.1093/nar/gkh121	journal	January 2004
HMMER web server: interactive sequence similarity searching Finn, R. D.; Clements, J.; Eddy, S. R. Nucleic Acids Research, Vol. 39, Issue suppl https://doi.org/10.1093/nar/gkr367	journal	May 2011
Metatranscriptomics Reveals the Diversity of Genes Expressed by Eukaryotes in Forest Soils Damon, Coralie; Lehembre, Frédéric; Oger-Desfeux, Christine PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0028967	journal	January 2012
Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific subtropical gyre Poretsky, Rachel S.; Hewson, Ian; Sun, Shulei Environmental Microbiology, Vol. 11, Issue 6 https://doi.org/10.1111/j.1462-2920.2008.01863.x	journal	June 2009
Regulation and characterization of Thermobifida fusca carbohydrate-binding module proteins E7 and E8 Moser, Felix; Irwin, Diana; Chen, Shaolin Biotechnology and Bioengineering, Vol. 100, Issue 6, p. 1066-1077 https://doi.org/10.1002/bit.21856	journal	January 2008
Next-generation biomass feedstocks for biofuel production Simmons, Blake A.; Loque, Dominique; Blanch, Harvey W. Genome Biology, Vol. 9, Issue 12 https://doi.org/10.1186/gb-2008-9-12-242	journal	January 2008
Changes in the actinomycetal communities during continuous thermophilic composting as revealed by denaturing gradient gel electrophoresis and quantitative PCR Xiao, Yong; Zeng, Guang-Ming; Yang, Zhao-Hui Bioresource Technology, Vol. 102, Issue 2 https://doi.org/10.1016/j.biortech.2010.09.034	journal	January 2011
The minimal enzyme cocktail concept for biomass processing Meyer, Anne S.; Rosgaard, Lisa; Sørensen, Hanne R. Journal of Cereal Science, Vol. 50, Issue 3 https://doi.org/10.1016/j.jcs.2009.01.010	journal	November 2009
Global potential bioethanol production from wasted crops and crop residues Kim, Seungdo; Dale, Bruce E. Biomass and Bioenergy, Vol. 26, Issue 4, p. 361-375 https://doi.org/10.1016/j.biombioe.2003.08.002	journal	April 2004
Thermostable Enzymes in Lignocellulose Hydrolysis Viikari, Liisa; Alapuranen, Marika; Puranen, Terhi Biofuels, p. 121-145 https://doi.org/10.1007/10_2007_065	book	January 2007
Microbial ecology of the Agaricus bisporus mushroom cropping process McGee, Conor F. Applied Microbiology and Biotechnology, Vol. 102, Issue 3 https://doi.org/10.1007/s00253-017-8683-9	journal	December 2017
Targeted A-to-G base editing of chloroplast DNA in plants Mok, Young Geun; Hong, Sunghyun; Bae, Su-Ji Nature Plants, Vol. 8, Issue 12 https://doi.org/10.1038/s41477-022-01279-8	journal	December 2022
Salinity tolerance mechanisms of an Arctic Pelagophyte using comparative transcriptomic and gene expression analysis Freyria, Nastasia J.; Kuo, Alan; Chovatia, Mansi Communications Biology, Vol. 5, Issue 1 https://doi.org/10.1038/s42003-022-03461-2	journal	May 2022
Diversity of Bacteria and Glycosyl Hydrolase Family 48 Genes in Cellulolytic Consortia Enriched from Thermophilic Biocompost Izquierdo, J. A.; Sizova, M. V.; Lynd, L. R. Applied and Environmental Microbiology, Vol. 76, Issue 11 https://doi.org/10.1128/aem.02689-09	journal	April 2010

Cited By (13)

Microbial community structure and dynamics in thermophilic composting viewed through metagenomics and metatranscriptomics Antunes, Luciana Principal; Martins, Layla Farage; Pereira, Roberta Verciano Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep38915	journal	December 2016
The initial soil microbiota impacts the potential for lignocellulose degradation during soil solarization Fernández‐Bayo, J. D.; Hestmark, K. V.; Claypool, J. T. Journal of Applied Microbiology, Vol. 126, Issue 6 https://doi.org/10.1111/jam.14258	journal	January 2019
Nutrient availability shapes the microbial community structure in sugarcane bagasse compost-derived consortia Mello, Bruno L.; Alessi, Anna M.; McQueen-Mason, Simon Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep38781	journal	December 2016
Targeted metatranscriptomics of compost-derived consortia reveals a GH11 exerting an unusual exo-1,4-β-xylanase activity Mello, Bruno L.; Alessi, Anna M.; Riaño-Pachón, Diego M. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0944-4	journal	November 2017
Structural Basis of Stereospecificity in the Bacterial Enzymatic Cleavage of β-Aryl Ether Bonds in Lignin Helmich, Kate E.; Pereira, Jose Henrique; Gall, Daniel L. Journal of Biological Chemistry, Vol. 291, Issue 10 https://doi.org/10.1074/jbc.m115.694307	journal	December 2015
Genome-Centric Analysis of a Thermophilic and Cellulolytic Bacterial Consortium Derived from Composting Lemos, Leandro N.; Pereira, Roberta V.; Quaggio, Ronaldo B. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00644	journal	April 2017
The structural and functional contributions of β-glucosidase-producing microbial communities to cellulose degradation in composting Zang, Xiangyun; Liu, Meiting; Fan, Yihong Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1045-8	journal	February 2018
The distribution of active β-glucosidase-producing microbial communities in composting Zang, Xiangyun; Liu, Meiting; Wang, Han Canadian Journal of Microbiology, Vol. 63, Issue 12 https://doi.org/10.1139/cjm-2017-0368	journal	December 2017
Metasecretome analysis of a lignocellulolytic microbial consortium grown on wheat straw, xylan and xylose Jiménez, Diego Javier; Maruthamuthu, Mukil; van Elsas, Jan Dirk Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0387-8	journal	December 2015
Characterization of three plant biomass-degrading microbial consortia by metagenomics- and metasecretomics-based approaches Jiménez, Diego Javier; de Lima Brossi, Maria Julia; Schückel, Julia Applied Microbiology and Biotechnology, Vol. 100, Issue 24 https://doi.org/10.1007/s00253-016-7713-3	journal	July 2016
Metagenomic mining pectinolytic microbes and enzymes from an apple pomace-adapted compost microbial community Zhou, Man; Guo, Peng; Wang, Tao Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0885-y	journal	August 2017
Discovery and characterization of a thermostable two-domain GH6 endoglucanase from a compost metagenome Jensen, Marianne S.; Fredriksen, Lasse; MacKenzie, Alasdair K. PLOS ONE, Vol. 13, Issue 5 https://doi.org/10.1371/journal.pone.0197862	journal	May 2018
Temporal Expression Dynamics of Plant Biomass-Degrading Enzymes by a Synthetic Bacterial Consortium Growing on Sugarcane Bagasse Jiménez, Diego Javier; Chaib De Mares, Maryam; Salles, Joana Falcão Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00299	journal	February 2018

Similar Records

Complete genome of the cellyloytic thermophile Acidothermus cellulolyticus 11B provides insights into its ecophysiological and evloutionary adaptations

Journal Article · Thu Jan 01 00:00:00 EST 2009 · Genome Research · OSTI ID:1257270

Barabote, Ravi D; Xie, Gary; Leu, David H; +14 more

Novel multidomain, multifunctional glycoside hydrolases from highly lignocellulolytic Caldicellulosiruptor species

Journal Article · Wed Jul 11 00:00:00 EDT 2018 · AIChE Journal · OSTI ID:1257270

Conway, Jonathan M.; Crosby, James R.; Hren, Andrew P.; +8 more

Deletion of Caldicellulosiruptor bescii CelA reveals its crucial role in the deconstruction of lignocellulosic biomass

Program Document · Thu Oct 09 00:00:00 EDT 2014 · Biotechnology for Biofuels · OSTI ID:1257270

Young, Jenna; Chung, Daehwan; Bomble, Yannick J.; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
lignocellulose deconstruction
solid-state culture
microbial communities
biofuels
cellulase
glycoside hydrolase family 48
carbohydrate binding module family 2
carbohydrate binding module family 33

Title: Metatranscriptomic analysis of lignocellulolytic microbial communities involved in high-solids decomposition of rice straw

Citation Formats

References (36)

Cited By (13)

Similar Records

Related Subjects