Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere

Doud, Devin F.  R.; Bowers, Robert M.; Schulz, Frederik; De Raad, Markus; Deng, Kai; Tarver, Angela; Glasgow, Evan; Vander Meulen, Kirk; Fox, Brian; Deutsch, Sam; Yoshikuni, Yasuo; Northen, Trent; Hedlund, Brian P.; Singer, Steven W.; Ivanova, Natalia; Woyke, Tanja

doi:10.1038/s41396-019-0557-y

Title: Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere

Journal Article · 21 November 2019 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-019-0557-y · OSTI ID:1609108

Doud, Devin F. R. ^[1]; Bowers, Robert M. ^[1];

^[1]; De Raad, Markus ^[2]; Deng, Kai ^[3]; Tarver, Angela ^[1]; Glasgow, Evan ^[4]; Vander Meulen, Kirk ^[4];

^[4]; Deutsch, Sam ^[1];

^[5];

^[6];

^[7];

^[5];

^[8]

USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Univ. of Wisconsin, Madison, WI (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of Nevada, Las Vegas, NV (United States)
Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Merced, CA (United States)

Assigning a functional role to a microorganism has historically relied on cultivation of isolates or detection of environmental genome-based biomarkers using a posteriori knowledge of function. However, the emerging field of function-driven single-cell genomics aims to expand this paradigm by identifying and capturing individual microbes based on their in situ functions or traits. To identify and characterize yet uncultivated microbial taxa involved in cellulose degradation, we developed and benchmarked a function-driven single-cell screen, which we applied to a microbial community inhabiting the Great Boiling Spring (GBS) Geothermal Field, northwest Nevada. Our approach involved recruiting microbes to fluorescently labeled cellulose particles, and then isolating single microbe-bound particles via fluorescence-activated cell sorting. The microbial community profiles prior to sorting were determined via bulk sample 16S rRNA gene amplicon sequencing. The flow-sorted cellulose-bound microbes were subjected to whole genome amplification and shotgun sequencing, followed by phylogenetic placement. Next, putative cellulase genes were identified, expressed and tested for activity against derivatives of cellulose and xylose. Alongside typical cellulose degraders, including members of the Actinobacteria, Bacteroidetes, and Chloroflexi, we found divergent cellulases encoded in the genome of a recently described candidate phylum from the rare biosphere, Goldbacteria, and validated their cellulase activity. As this genome represents a species-level organism with novel and phylogenetically distinct cellulolytic activity, we propose the name Candidatus ‘Cellulosimonas argentiregionis’. We expect that this function-driven single-cell approach can be extended to a broad range of substrates, linking microbial taxonomy directly to in situ function.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States); Joint BioEnergy Institute (JBEI), Emeryville, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; SC0018409; FC02- 07ER64494

OSTI ID:: 1609108

Alternate ID(s):: OSTI ID: 1579340

Journal Information:: The ISME Journal, Vol. 14, Issue 3; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 42 works

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References (139)

Analysis of immune, microbiota and metabolome maturation in infants in a clinical trial of Lactobacillus paracasei CBA L74-fermented formula Roggero, Paola; Liotto, Nadia; Pozzi, Chiara Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-16582-1	journal	June 2020
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
Turning up the heat on biomass degradation Jermy, Andrew Nature Reviews Microbiology, Vol. 9, Issue 9 https://doi.org/10.1038/nrmicro2639	journal	August 2011
Ecology and exploration of the rare biosphere Lynch, Michael D. J.; Neufeld, Josh D. Nature Reviews Microbiology, Vol. 13, Issue 4 https://doi.org/10.1038/nrmicro3400	journal	March 2015
Shifting the genomic gold standard for the prokaryotic species definition Richter, Michael; Rosselló-Móra, Ramon Proceedings of the National Academy of Sciences, Vol. 106, Issue 45 https://doi.org/10.1073/pnas.0906412106	journal	October 2009
Genomics of Aerobic Cellulose Utilization Systems in Actinobacteria Anderson, Iain; Abt, Birte; Lykidis, Athanasios PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0039331	journal	June 2012
Periplasmic Cytophaga hutchinsonii Endoglucanases Are Required for Use of Crystalline Cellulose as the Sole Source of Carbon and Energy Zhu, Yongtao; Han, Lanlan; Hefferon, Kathleen L. Applied and Environmental Microbiology, Vol. 82, Issue 15 https://doi.org/10.1128/AEM.01298-16	journal	June 2016
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 35, Issue 8 https://doi.org/10.1038/nbt.3893	journal	August 2017
Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity Hugenholtz, Philip; Goebel, Brett M.; Pace, Norman R. Journal of Bacteriology, Vol. 180, Issue 18 https://doi.org/10.1128/JB.180.18.4765-4774.1998	journal	September 1998
The candidate phylum â€˜Termite Group 1â€™ of bacteria: phylogenetic diversity, distribution, and endosymbiont members of various gut flagellated protists: Investigation of bacterial phylum Termite Group 1 Ohkuma, Moriya; Sato, Tomoyuki; Noda, Satoko FEMS Microbiology Ecology, Vol. 60, Issue 3 https://doi.org/10.1111/j.1574-6941.2007.00311.x	journal	June 2007
RNAmmer: consistent and rapid annotation of ribosomal RNA genes Lagesen, Karin; Hallin, Peter; Rødland, Einar Andreas Nucleic Acids Research, Vol. 35, Issue 9 https://doi.org/10.1093/nar/gkm160	journal	April 2007
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
genoPlotR: comparative gene and genome visualization in R Guy, L.; Roat Kultima, J.; Andersson, S. G. E. Bioinformatics, Vol. 26, Issue 18 https://doi.org/10.1093/bioinformatics/btq413	journal	July 2010
Characterization of All Family-9 Glycoside Hydrolases Synthesized by the Cellulosome-producing Bacterium Clostridium cellulolyticum Ravachol, Julie; Borne, Romain; Tardif, Chantal Journal of Biological Chemistry, Vol. 289, Issue 11 https://doi.org/10.1074/jbc.M113.545046	journal	January 2014
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Rare species contribute disproportionately to the functional structure of species assemblages Leitão, Rafael P.; Zuanon, Jansen; Villéger, Sébastien Proceedings of the Royal Society B: Biological Sciences, Vol. 283, Issue 1828 https://doi.org/10.1098/rspb.2016.0084	journal	April 2016
Cell-Free Translation of Biofuel Enzymes Takasuka, Taichi E.; Walker, Johnnie A.; Bergeman, Lai F. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-782-2_5	book	December 2013
Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community Robert, C.; Chassard, C.; Lawson, P. A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 7 https://doi.org/10.1099/ijs.0.64998-0	journal	July 2007
Stable isotope probing in the metagenomics era: A bridge towards improved bioremediation Uhlik, Ondrej; Leewis, Mary-Cathrine; Strejcek, Michal Biotechnology Advances, Vol. 31, Issue 2 https://doi.org/10.1016/j.biotechadv.2012.09.003	journal	March 2013
A Comprehensive Census of Microbial Diversity in Hot Springs of Tengchong, Yunnan Province China Using 16S rRNA Gene Pyrosequencing Hou, Weiguo; Wang, Shang; Dong, Hailiang PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0053350	journal	January 2013
Primer and platform effects on 16S rRNA tag sequencing Alison, Fern,; Feng, Chen,; Julien, Tremblay, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/wgfs-e050	text	January 2015
Where less may be more: how the rare biosphere pulls ecosystems strings Jousset, Alexandre; Rillig, Matthias C.; Bienhold, Christina Freie Universität Berlin https://doi.org/10.17169/refubium-25396	text	January 2017
Uncultivated thermophiles: current status and spotlight on ‘Aigarchaeota’ Hedlund, Brian P.; Murugapiran, Senthil K.; Alba, Timothy W. Current Opinion in Microbiology, Vol. 25 https://doi.org/10.1016/j.mib.2015.06.008	journal	June 2015
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments Hernsdorf, Alex W.; Amano, Yuki; Miyakawa, Kazuya The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.39	journal	March 2017
BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments Criscuolo, Alexis; Gribaldo, Simonetta BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-210	journal	January 2010
CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T. Genome Research, Vol. 25, Issue 7 https://doi.org/10.1101/gr.186072.114	journal	May 2015
Reconstructing each cell's genome within complex microbial communitiesâ€”dream or reality? Clingenpeel, Scott; Clum, Alicia; Schwientek, Patrick Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00771	journal	January 2015
Rapid Kinetic Characterization of Glycosyl Hydrolases Based on Oxime Derivatization and Nanostructure-Initiator Mass Spectrometry (NIMS) Deng, Kai; Takasuka, Taichi E.; Heins, Richard ACS Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1021/cb5000289	journal	May 2014
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences Li, W.; Godzik, A. Bioinformatics, Vol. 22, Issue 13 https://doi.org/10.1093/bioinformatics/btl158	journal	May 2006
Quantitative Microbial Ecology through Stable Isotope Probing Hungate, Bruce A.; Mau, Rebecca L.; Schwartz, Egbert Applied and Environmental Microbiology, Vol. 81, Issue 21 https://doi.org/10.1128/AEM.02280-15	journal	August 2015
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
Kallotenue papyrolyticum gen. nov., sp. nov., a cellulolytic and filamentous thermophile that represents a novel lineage (Kallotenuales ord. nov., Kallotenuaceae fam. nov.) within the class Chloroflexia Cole, J. K.; Gieler, B. A.; Heisler, D. L. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 12 https://doi.org/10.1099/ijs.0.053348-0	journal	August 2013
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle Proceedings of the National Academy of Sciences, Vol. 113, Issue 28 https://doi.org/10.1073/pnas.1603757113	journal	June 2016
Cellulases: ambiguous nonhomologous enzymes in a genomic perspective Sukharnikov, Leonid O.; Cantwell, Brian J.; Podar, Mircea Trends in Biotechnology, Vol. 29, Issue 10 https://doi.org/10.1016/j.tibtech.2011.04.008	journal	October 2011
An automated Raman-based platform for the sorting of live cells by functional properties Lee, Kang Soo; Palatinszky, Márton; Pereira, Fátima C. Nature Microbiology, Vol. 4, Issue 6 https://doi.org/10.1038/s41564-019-0394-9	journal	March 2019
Pyrosequencing Reveals High-Temperature Cellulolytic Microbial Consortia in Great Boiling Spring after In Situ Lignocellulose Enrichment Peacock, Joseph P.; Cole, Jessica K.; Murugapiran, Senthil K. PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0059927	journal	March 2013
Erratum: Corrigendum: Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 36, Issue 7 https://doi.org/10.1038/nbt0718-660a	journal	July 2018
Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs Eloe-Fadrosh, Emiley A.; Paez-Espino, David; Jarett, Jessica Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10476	journal	January 2016
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes Pruesse, Elmar; Peplies, Jörg; Glöckner, Frank Oliver Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts252	journal	May 2012
Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia Martinez-Garcia, Manuel; Brazel, David M.; Swan, Brandon K. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035314	journal	April 2012
Decontamination of MDA Reagents for Single Cell Whole Genome Amplification Woyke, Tanja; Sczyrba, Alexander; Lee, Janey PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0026161	journal	October 2011
Where less may be more: how the rare biosphere pulls ecosystems strings Jousset, Alexandre; Bienhold, Christina; Chatzinotas, Antonis The ISME Journal, Vol. 11, Issue 4 https://doi.org/10.1038/ismej.2016.174	journal	January 2017
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Stable isotope probing — linking microbial identity to function Dumont, Marc G.; Murrell, J. Colin Nature Reviews Microbiology, Vol. 3, Issue 6 https://doi.org/10.1038/nrmicro1162	journal	May 2005
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Deletion of the Cytophaga hutchinsonii type IX secretion system gene sprP results in defects in gliding motility and cellulose utilization Zhu, Yongtao; McBride, Mark J. Applied Microbiology and Biotechnology, Vol. 98, Issue 2 https://doi.org/10.1007/s00253-013-5355-2	journal	November 2013
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky901	journal	October 2018
Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles Stepanauskas, Ramunas; Fergusson, Elizabeth A.; Brown, Joseph Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00128-z	journal	July 2017
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics Rinke, Christian; Lee, Janey; Nath, Nandita Nature Protocols, Vol. 9, Issue 5 https://doi.org/10.1038/nprot.2014.067	journal	April 2014
Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria , and a proposal of a novel bacterial phylum I gnavibacteriae Podosokorskaya, Olga A.; Kadnikov, Vitaly V.; Gavrilov, Sergey N. Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12067	journal	January 2013
Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea Yelton, Alexis P.; Comolli, Luis R.; Justice, Nicholas B. BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-485	journal	January 2013
Genomic Analysis of "Elusimicrobium minutum," the First Cultivated Representative of the Phylum "Elusimicrobia" (Formerly Termite Group 1) Herlemann, D. P. R.; Geissinger, O.; Ikeda-Ohtsubo, W. Applied and Environmental Microbiology, Vol. 75, Issue 9 https://doi.org/10.1128/AEM.02698-08	journal	March 2009
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E. The ISME Journal, Vol. 15, Issue 8 https://doi.org/10.1038/s41396-021-00921-1	journal	March 2021
Visualizing in situ translational activity for identifying and sorting slow-growing archaeal−bacterial consortia Hatzenpichler, Roland; Connon, Stephanie A.; Goudeau, Danielle Proceedings of the National Academy of Sciences, Vol. 113, Issue 28 https://doi.org/10.1073/pnas.1603757113	journal	June 2016
ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data Yu, Guangchuang; Smith, David K.; Zhu, Huachen Methods in Ecology and Evolution, Vol. 8, Issue 1 https://doi.org/10.1111/2041-210X.12628	journal	September 2016
Author Correction: Improved genome recovery and integrated cell-size analyses of individual uncultured microbial cells and viral particles Stepanauskas, Ramunas; Fergusson, Elizabeth A.; Brown, Joseph Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02128-5	journal	December 2017
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
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
Genomics of cellulosic biofuels Rubin, Edward M. Nature, Vol. 454, Issue 7206 https://doi.org/10.1038/nature07190	journal	August 2008
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
OpenMSI Arrayed Analysis Toolkit: Analyzing Spatially Defined Samples Using Mass Spectrometry Imaging de Raad, Markus; de Rond, Tristan; Rübel, Oliver Analytical Chemistry, Vol. 89, Issue 11 https://doi.org/10.1021/acs.analchem.6b05004	journal	May 2017
Clathrate nanostructures for mass spectrometry Northen, Trent R.; Yanes, Oscar; Northen, Michael T. Nature, Vol. 449, Issue 7165 https://doi.org/10.1038/nature06195	journal	October 2007
BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments Criscuolo, Alexis; Gribaldo, Simonetta BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-210	journal	January 2010
Cellulases and their interaction with cellulose Henrissat, Bernard Cellulose, Vol. 1, Issue 3 https://doi.org/10.1007/BF00813506	journal	September 1994
Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3120	journal	August 2013
Complete Genome Sequence of Endomicrobium proavitum , a Free-Living Relative of the Intracellular Symbionts of Termite Gut Flagellates (Phylum Elusimicrobia ) Zheng, Hao; Brune, Andreas Genome Announcements, Vol. 3, Issue 4 https://doi.org/10.1128/genomeA.00679-15	journal	July 2015
Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia Gary, Xie,; K., Swan, Brandon; G., Chain, Patrick S. The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/fzc0-xq44	text	January 2012
Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community Robert, C.; Chassard, C.; Lawson, P. A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 7 https://doi.org/10.1099/ijs.0.64998-0	journal	July 2007
Cellulases: ambiguous nonhomologous enzymes in a genomic perspective Sukharnikov, Leonid O.; Cantwell, Brian J.; Podar, Mircea Trends in Biotechnology, Vol. 29, Issue 10 https://doi.org/10.1016/j.tibtech.2011.04.008	journal	October 2011
Novel High-Rank Phylogenetic Lineages within a Sulfur Spring (Zodletone Spring, Oklahoma), Revealed Using a Combined Pyrosequencing-Sanger Approach Youssef, Noha; Steidley, Brandi L.; Elshahed, Mostafa S. Applied and Environmental Microbiology, Vol. 78, Issue 8 https://doi.org/10.1128/AEM.00002-12	journal	February 2012
Genomics of Aerobic Cellulose Utilization Systems in Actinobacteria Anderson, Iain; Abt, Birte; Lykidis, Athanasios PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0039331	journal	June 2012
Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment Castelle, Cindy J.; Hug, Laura A.; Wrighton, Kelly C. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3120	journal	August 2013
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences Li, W.; Godzik, A. Bioinformatics, Vol. 22, Issue 13 https://doi.org/10.1093/bioinformatics/btl158	journal	May 2006
Active Site and Laminarin Binding in Glycoside Hydrolase Family 55 Bianchetti, Christopher M.; Takasuka, Taichi E.; Deutsch, Sam Journal of Biological Chemistry, Vol. 290, Issue 19 https://doi.org/10.1074/jbc.M114.623579	journal	March 2015
Rapid Kinetic Characterization of Glycosyl Hydrolases Based on Oxime Derivatization and Nanostructure-Initiator Mass Spectrometry (NIMS) Deng, Kai; Takasuka, Taichi E.; Heins, Richard ACS Chemical Biology, Vol. 9, Issue 7 https://doi.org/10.1021/cb5000289	journal	May 2014
Phylogenetic Distribution of Potential Cellulases in Bacteria Berlemont, Renaud; Martiny, Adam C. Applied and Environmental Microbiology, Vol. 79, Issue 5 https://doi.org/10.1128/AEM.03305-12	journal	December 2012
Characterization of the cellulolytic complex (cellulosome) produced by Clostridium cellulolyticum. Gal, L.; Pages, S.; Gaudin, C. Applied and environmental microbiology, Vol. 63, Issue 3 https://doi.org/10.1128/AEM.63.3.903-909.1997	journal	January 1997
Identification of groups of metabolically-active rhizosphere microorganisms by stable isotope probing of PLFAs Treonis, Amy M.; Ostle, Nick J.; Stott, Andrew W. Soil Biology and Biochemistry, Vol. 36, Issue 3 https://doi.org/10.1016/j.soilbio.2003.10.015	journal	March 2004
Identification and characterization of a multidomain hyperthermophilic cellulase from an archaeal enrichment Graham, Joel E.; Clark, Melinda E.; Nadler, Dana C. Nature Communications, Vol. 2, Issue 1 https://doi.org/10.1038/ncomms1373	journal	July 2011
Uncultivated thermophiles: current status and spotlight on ‘Aigarchaeota’ Hedlund, Brian P.; Murugapiran, Senthil K.; Alba, Timothy W. Current Opinion in Microbiology, Vol. 25 https://doi.org/10.1016/j.mib.2015.06.008	journal	June 2015
Clathrate nanostructures for mass spectrometry Northen, Trent R.; Yanes, Oscar; Northen, Michael T. Nature, Vol. 449, Issue 7165 https://doi.org/10.1038/nature06195	journal	October 2007
Ecology and exploration of the rare biosphere Lynch, Michael D. J.; Neufeld, Josh D. Nature Reviews Microbiology, Vol. 13, Issue 4 https://doi.org/10.1038/nrmicro3400	journal	March 2015
Cellulosomal Scaffoldin-Like Proteins from Ruminococcus flavefaciens Ding, S. -Y.; Rincon, M. T.; Lamed, R. Journal of Bacteriology, Vol. 183, Issue 6 https://doi.org/10.1128/JB.183.6.1945-1953.2001	journal	March 2001
Kallotenue papyrolyticum gen. nov., sp. nov., a cellulolytic and filamentous thermophile that represents a novel lineage (Kallotenuales ord. nov., Kallotenuaceae fam. nov.) within the class Chloroflexia Cole, J. K.; Gieler, B. A.; Heisler, D. L. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 63, Issue Pt 12 https://doi.org/10.1099/ijs.0.053348-0	journal	August 2013
Potential for microbial H2 and metal transformations associated with novel bacteria and archaea in deep terrestrial subsurface sediments Hernsdorf, Alex W.; Amano, Yuki; Miyakawa, Kazuya The ISME Journal, Vol. 11, Issue 8 https://doi.org/10.1038/ismej.2017.39	journal	March 2017
Community Microrespirometry and Molecular Analyses Reveal a Diverse Energy Economy in Great Boiling Spring and Sandy's Spring West in the U.S. Great Basin Murphy, Caitlin N.; Dodsworth, Jeremy A.; Babbitt, Aaron B. Applied and Environmental Microbiology, Vol. 79, Issue 10 https://doi.org/10.1128/AEM.00139-13	journal	March 2013
Development of a High Throughput Platform for Screening Glycoside Hydrolases Based on Oxime-NIMS Deng, Kai; Guenther, Joel M.; Gao, Jian Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00153	journal	October 2015
Clostridium cellulolyticum : model organism of mesophilic cellulolytic clostridia Desvaux, Mickaël FEMS Microbiology Reviews, Vol. 29, Issue 4 https://doi.org/10.1016/j.femsre.2004.11.003	journal	September 2005
A Comprehensive Census of Microbial Diversity in Hot Springs of Tengchong, Yunnan Province China Using 16S rRNA Gene Pyrosequencing Hou, Weiguo; Wang, Shang; Dong, Hailiang PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0053350	journal	January 2013
Where less may be more: how the rare biosphere pulls ecosystems strings Jousset, Alexandre; Rillig, Matthias C.; Bienhold, Christina Freie Universität Berlin https://doi.org/10.17169/refubium-25396	text	January 2017
Molecular characterization of lumpy skin disease virus (LSDV) emerged in Bangladesh reveals unique genetic features compared to contemporary field strains Badhy, Shukes Chandra; Chowdhury, Mohammad Golam Azam; Settypalli, Tirumala Bharani Kumar BMC Veterinary Research, Vol. 17, Issue 1 https://doi.org/10.1186/s12917-021-02751-x	journal	January 2021
Pfam: the protein families database Finn, Robert D.; Bateman, Alex; Clements, Jody Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1223	journal	November 2013
OpenMSI Arrayed Analysis Toolkit: Analyzing Spatially Defined Samples Using Mass Spectrometry Imaging de Raad, Markus; de Rond, Tristan; Rübel, Oliver Analytical Chemistry, Vol. 89, Issue 11 https://doi.org/10.1021/acs.analchem.6b05004	journal	May 2017
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Tracking heavy water (D ₂ O) incorporation for identifying and sorting active microbial cells Berry, David; Mader, Esther; Lee, Tae Kwon Proceedings of the National Academy of Sciences, Vol. 112, Issue 2 https://doi.org/10.1073/pnas.1420406112	journal	December 2014
Novel approaches in function-driven single-cell genomics Doud, Devin F. R.; Woyke, Tanja FEMS Microbiology Reviews, Vol. 41, Issue 4 https://doi.org/10.1093/femsre/fux009	journal	June 2017
E ndomicrobium proavitum , the first isolate of E ndomicrobia class. nov. (phylum E lusimicrobia ) - an ultramicrobacterium with an unusual cell cycle that fixes nitrogen with a Group IV nitrogenase Zheng, Hao; Dietrich, Carsten; Radek, Renate Environmental Microbiology, Vol. 18, Issue 1 https://doi.org/10.1111/1462-2920.12960	journal	July 2015
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt Molecular Biology and Evolution, Vol. 32, Issue 1 https://doi.org/10.1093/molbev/msu300	journal	November 2014
Biomass pretreatment: Fundamentals toward application Agbor, Valery B.; Cicek, Nazim; Sparling, Richard Biotechnology Advances, Vol. 29, Issue 6 https://doi.org/10.1016/j.biotechadv.2011.05.005	journal	November 2011
Horizontal Gene Transfer as an Indispensable Driver for Evolution of Neocallimastigomycota into a Distinct Gut-Dwelling Fungal Lineage Murphy, Chelsea L.; Youssef, Noha H.; Hanafy, Radwa A. Applied and Environmental Microbiology, Vol. 85, Issue 15 https://doi.org/10.1128/AEM.00988-19	journal	May 2019
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea Yelton, Alexis P.; Comolli, Luis R.; Justice, Nicholas B. BMC Genomics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2164-14-485	journal	January 2013
ARB: a software environment for sequence data Ludwig, W. Nucleic Acids Research, Vol. 32, Issue 4 https://doi.org/10.1093/nar/gkh293	journal	February 2004
Capturing Single Cell Genomes of Active Polysaccharide Degraders: An Unexpected Contribution of Verrucomicrobia Martinez-Garcia, Manuel; Brazel, David M.; Swan, Brandon K. PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035314	journal	April 2012
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes Pruesse, Elmar; Peplies, Jörg; Glöckner, Frank Oliver Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts252	journal	May 2012
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
The carbohydrate-active enzymes database (CAZy) in 2013 Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1178	journal	November 2013
Genomics of cellulosic biofuels Rubin, Edward M. Nature, Vol. 454, Issue 7206 https://doi.org/10.1038/nature07190	journal	August 2008
Pyrosequencing Reveals High-Temperature Cellulolytic Microbial Consortia in Great Boiling Spring after In Situ Lignocellulose Enrichment Peacock, Joseph P.; Cole, Jessica K.; Murugapiran, Senthil K. PLoS ONE, Vol. 8, Issue 3 https://doi.org/10.1371/journal.pone.0059927	journal	March 2013
An automated Raman-based platform for the sorting of live cells by functional properties Lee, Kang Soo; Palatinszky, Márton; Pereira, Fátima C. Nature Microbiology, Vol. 4, Issue 6 https://doi.org/10.1038/s41564-019-0394-9	journal	March 2019
Global metagenomic survey reveals a new bacterial candidate phylum in geothermal springs Eloe-Fadrosh, Emiley A.; Paez-Espino, David; Jarett, Jessica Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10476	journal	January 2016
Stable isotope probing — linking microbial identity to function Dumont, Marc G.; Murrell, J. Colin Nature Reviews Microbiology, Vol. 3, Issue 6 https://doi.org/10.1038/nrmicro1162	journal	May 2005
Tracking heavy water (D ₂ O) incorporation for identifying and sorting active microbial cells Berry, David; Mader, Esther; Lee, Tae Kwon Proceedings of the National Academy of Sciences, Vol. 112, Issue 2 https://doi.org/10.1073/pnas.1420406112	journal	December 2014
Genome Sequence of the Cellulolytic Gliding Bacterium Cytophaga hutchinsonii Xie, G.; Bruce, D. C.; Challacombe, J. F. Applied and Environmental Microbiology, Vol. 73, Issue 11 https://doi.org/10.1128/AEM.00225-07	journal	March 2007
High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07641-9	journal	November 2018
Single-cell bacterial transcription measurements reveal the importance of dimethylsulfoniopropionate (DMSP) hotspots in ocean sulfur cycling Gao, Cherry; Fernandez, Vicente I.; Lee, Kang S. ETH Zurich https://doi.org/10.3929/ethz-b-000412734	text	January 2020
Stable isotope probing in the metagenomics era: A bridge towards improved bioremediation Uhlik, Ondrej; Leewis, Mary-Cathrine; Strejcek, Michal Biotechnology Advances, Vol. 31, Issue 2 https://doi.org/10.1016/j.biotechadv.2012.09.003	journal	March 2013
Cell-Free Translation of Biofuel Enzymes Takasuka, Taichi E.; Walker, Johnnie A.; Bergeman, Lai F. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-782-2_5	book	December 2013
Obtaining genomes from uncultivated environmental microorganisms using FACS–based single-cell genomics Rinke, Christian; Lee, Janey; Nath, Nandita Nature Protocols, Vol. 9, Issue 5 https://doi.org/10.1038/nprot.2014.067	journal	April 2014
Biomass pretreatment: Fundamentals toward application Agbor, Valery B.; Cicek, Nazim; Sparling, Richard Biotechnology Advances, Vol. 29, Issue 6 https://doi.org/10.1016/j.biotechadv.2011.05.005	journal	November 2011
IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna Nucleic Acids Research, Vol. 47, Issue D1 https://doi.org/10.1093/nar/gky901	journal	October 2018
Novel approaches in function-driven single-cell genomics Doud, Devin F. R.; Woyke, Tanja FEMS Microbiology Reviews, Vol. 41, Issue 4 https://doi.org/10.1093/femsre/fux009	journal	June 2017
Microfluidic-based mini-metagenomics enables discovery of novel microbial lineages from complex environmental samples Yu, Feiqiao Brian; Blainey, Paul C.; Schulz, Frederik eLife, Vol. 6 https://doi.org/10.7554/eLife.26580	journal	July 2017
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Genome Sequence of the Polysaccharide-Degrading, Thermophilic Anaerobe Spirochaeta thermophila DSM 6192 Angelov, A.; Liebl, S.; Ballschmiter, M. Journal of Bacteriology, Vol. 192, Issue 24 https://doi.org/10.1128/JB.01023-10	journal	October 2010
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria , and a proposal of a novel bacterial phylum I gnavibacteriae Podosokorskaya, Olga A.; Kadnikov, Vitaly V.; Gavrilov, Sergey N. Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12067	journal	January 2013
Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae) Hongoh, Yuichi; Ohkuma, Moriya; Kudo, Toshiaki FEMS Microbiology Ecology, Vol. 44, Issue 2 https://doi.org/10.1016/S0168-6496(03)00026-6	journal	May 2003
Development of a High Throughput Platform for Screening Glycoside Hydrolases Based on Oxime-NIMS Deng, Kai; Guenther, Joel M.; Gao, Jian Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00153	journal	October 2015
Primer and platform effects on 16S rRNA tag sequencing Tremblay, Julien; Singh, Kanwar; Fern, Alison Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00771	journal	August 2015

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