Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression
Abstract
In this study, the evolution of cellulose degradation was a defining event in the history of life. Without efficient decomposition and recycling, dead plant biomass would quickly accumulate and become inaccessible to terrestrial food webs and the global carbon cycle. On land, the primary drivers of plant biomass deconstruction are fungi and bacteria in the soil or associated with herbivorous eukaryotes. While the ecological importance of plant-decomposing microbes is well established, little is known about the distribution or evolution of cellulolytic activity in any bacterial genus. Here we show that in Streptomyces, a genus of Actinobacteria abundant in soil and symbiotic niches, the ability to rapidly degrade cellulose is largely restricted to two clades of host-associated strains and is not a conserved characteristic of the Streptomyces genus or host-associated strains. Our comparative genomics identify that while plant biomass degrading genes (CAZy) are widespread in Streptomyces, key enzyme families are enriched in highly cellulolytic strains. Transcriptomic analyses demonstrate that cellulolytic strains express a suite of multi-domain CAZy enzymes that are coregulated by the CebR transcriptional regulator. Using targeted gene deletions, we verify the importance of a highly expressed cellulase (GH6 family cellobiohydrolase) and the CebR transcriptional repressor to the cellulolytic phenotype.more »
- Authors:
-
[1];
[1];
- Univ. of Wisconsin-Madison, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center and Dept. of Bacteriology
- Univ. of Wisconsin-Madison, Madison, WI (United States). DOE Great Lakes Bioenergy Research Center and Dept. of Biochemistry
- Univ. of Wisconsin-Madison, Madison, WI (United States). Dept. of Entomology
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1287326
- Grant/Contract Number:
- FC02-07ER64494; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Biology (Online)
- Additional Journal Information:
- Journal Name: PLoS Biology (Online); Journal Volume: 14; Journal Issue: 6; Journal ID: ISSN 1545-7885
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; lytic polysaccharide monooxygenases; multiple sequence alignment; functional-characterization; phylogenetic analysis; transport-system; binding-protein; fungal genomes; reticuli; soil; cellulases; streptomyces; cellulose; plant genomics; evolutionary genetics; gene expression; sequence motif analysis; fungal evolution
Citation Formats
Book, Adam J., Lewin, Gina R., McDonald, Bradon R., Takasuka, Taichi E., Wendt-Pienkowski, Evelyn, Doering, Drew T., Suh, Steven, Raffa, Kenneth F., Fox, Brian G., and Currie, Cameron R. Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. United States: N. p., 2016.
Web. doi:10.1371/journal.pbio.1002475.
Book, Adam J., Lewin, Gina R., McDonald, Bradon R., Takasuka, Taichi E., Wendt-Pienkowski, Evelyn, Doering, Drew T., Suh, Steven, Raffa, Kenneth F., Fox, Brian G., & Currie, Cameron R. Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression. United States. https://doi.org/10.1371/journal.pbio.1002475
Book, Adam J., Lewin, Gina R., McDonald, Bradon R., Takasuka, Taichi E., Wendt-Pienkowski, Evelyn, Doering, Drew T., Suh, Steven, Raffa, Kenneth F., Fox, Brian G., and Currie, Cameron R. Wed .
"Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression". United States. https://doi.org/10.1371/journal.pbio.1002475. https://www.osti.gov/servlets/purl/1287326.
@article{osti_1287326,
title = {Evolution of high cellulolytic activity in symbiotic Streptomyces through selection of expanded gene content and coordinated gene expression},
author = {Book, Adam J. and Lewin, Gina R. and McDonald, Bradon R. and Takasuka, Taichi E. and Wendt-Pienkowski, Evelyn and Doering, Drew T. and Suh, Steven and Raffa, Kenneth F. and Fox, Brian G. and Currie, Cameron R.},
abstractNote = {In this study, the evolution of cellulose degradation was a defining event in the history of life. Without efficient decomposition and recycling, dead plant biomass would quickly accumulate and become inaccessible to terrestrial food webs and the global carbon cycle. On land, the primary drivers of plant biomass deconstruction are fungi and bacteria in the soil or associated with herbivorous eukaryotes. While the ecological importance of plant-decomposing microbes is well established, little is known about the distribution or evolution of cellulolytic activity in any bacterial genus. Here we show that in Streptomyces, a genus of Actinobacteria abundant in soil and symbiotic niches, the ability to rapidly degrade cellulose is largely restricted to two clades of host-associated strains and is not a conserved characteristic of the Streptomyces genus or host-associated strains. Our comparative genomics identify that while plant biomass degrading genes (CAZy) are widespread in Streptomyces, key enzyme families are enriched in highly cellulolytic strains. Transcriptomic analyses demonstrate that cellulolytic strains express a suite of multi-domain CAZy enzymes that are coregulated by the CebR transcriptional regulator. Using targeted gene deletions, we verify the importance of a highly expressed cellulase (GH6 family cellobiohydrolase) and the CebR transcriptional repressor to the cellulolytic phenotype. Evolutionary analyses identify complex genomic modifications that drive plant biomass deconstruction in Streptomyces, including acquisition and selective retention of CAZy genes and transcriptional regulators. Our results suggest that host-associated niches have selected some symbiotic Streptomyces for increased cellulose degrading activity and that symbiotic bacteria are a rich biochemical and enzymatic resource for biotechnology.},
doi = {10.1371/journal.pbio.1002475},
journal = {PLoS Biology (Online)},
number = 6,
volume = 14,
place = {United States},
year = {Wed Jun 08 00:00:00 EDT 2016},
month = {Wed Jun 08 00:00:00 EDT 2016}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 50 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases
journal, January 2014
- Book, Adam J.; Yennamalli, Ragothaman M.; Takasuka, Taichi E.
- Biotechnology for Biofuels, Vol. 7, Issue 1
FIMO: scanning for occurrences of a given motif
journal, February 2011
- Grant, Charles E.; Bailey, Timothy L.; Noble, William Stafford
- Bioinformatics, Vol. 27, Issue 7
Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes
journal, April 2011
- Pullan, Steven T.; Chandra, Govind; Bibb, Mervyn J.
- BMC Genomics, Vol. 12, Issue 1
The Prokaryotes
book, January 1992
- Balows, Albert; Trüper, Hans G.; Dworkin, Martin
- Springer New York, NY
Genomics of Aerobic Cellulose Utilization Systems in Actinobacteria
journal, June 2012
- Anderson, Iain; Abt, Birte; Lykidis, Athanasios
- PLoS ONE, Vol. 7, Issue 6
The Cellobiose Sensor CebR Is the Gatekeeper of Streptomyces scabies Pathogenicity
journal, February 2015
- Francis, Isolde M.; Jourdan, Samuel; Fanara, Steven
- mBio, Vol. 6, Issue 2
Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria
journal, January 2001
- Chen, Junqin; Weimer, Paul J.
- Microbiology, Vol. 147, Issue 1
MEME: discovering and analyzing DNA and protein sequence motifs
journal, July 2006
- Bailey, T. L.; Williams, N.; Misleh, C.
- Nucleic Acids Research, Vol. 34, Issue Web Server
Production of the antitumor drug epirubicin (4′-epidoxorubicin) and its precursor by a genetically engineered strain of Streptomyces peucetius
journal, January 1998
- Madduri, Krishnamurthy; Kennedy, Jonathan; Rivola, Giovanni
- Nature Biotechnology, Vol. 16, Issue 1
Accounting For Alignment Uncertainty in Phylogenomics
journal, January 2012
- Wu, Martin; Chatterji, Sourav; Eisen, Jonathan A.
- PLoS ONE, Vol. 7, Issue 1
Production and characterization of multiple cellulolytic enzymes by isolated Streptomyces sp. MDS
journal, December 2012
- Saratale, Ganesh D.; Saratale, Rijuta G.; Oh, Sang Eun
- Biomass and Bioenergy, Vol. 47
Phylogenetic Distribution of Potential Cellulases in Bacteria
journal, December 2012
- Berlemont, Renaud; Martiny, Adam C.
- Applied and Environmental Microbiology, Vol. 79, Issue 5
I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010
- Roy, Ambrish; Kucukural, Alper; Zhang, Yang
- Nature Protocols, Vol. 5, Issue 4
An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides
journal, October 2010
- Vaaje-Kolstad, Gustav; Westereng, Bjørge; Horn, Svein J.
- Science, Vol. 330, Issue 6001, p. 219-222
Comparative genomics of actinomycetes with a focus on natural product biosynthetic genes
journal, January 2013
- Doroghazi, James R.; Metcalf, William W.
- BMC Genomics, Vol. 14, Issue 1
Estimating divergence times in large molecular phylogenies
journal, November 2012
- Tamura, K.; Battistuzzi, F. U.; Billing-Ross, P.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 47
Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces
journal, January 2013
- Takasuka, Taichi E.; Book, Adam J.; Lewin, Gina R.
- Scientific Reports, Vol. 3, Issue 1
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007
- Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
- Science, Vol. 315, Issue 5813, p. 804-807
Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi
journal, January 2013
- Zhao, Zhongtao; Liu, Huiquan; Wang, Chenfang
- BMC Genomics, Vol. 14, Issue 1
Cellulose-degrading bacteria associated with the invasive woodwasp Sirex noctilio
journal, March 2011
- Adams, Aaron S.; Jordan, Michelle S.; Adams, Sandye M.
- The ISME Journal, Vol. 5, Issue 8
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences
journal, February 2016
- Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae
- Journal of Molecular Biology, Vol. 428, Issue 4
A Lipid-Anchored Binding Protein is a Component of an ATP-Dependent Cellobiose/Cellotriose-Transport System from the Cellulose Degrader Streptomyces reticuli
journal, December 1996
- Schlosser, Andreas; Schrempf, Hildgund
- European Journal of Biochemistry, Vol. 242, Issue 2
Exploring the Potential for Actinobacteria as Defensive Symbionts in Fungus-Growing Termites
journal, December 2011
- Visser, Anna A.; Nobre, Tânia; Currie, Cameron R.
- Microbial Ecology, Vol. 63, Issue 4
Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp.
journal, July 1992
- Bierman, M.; Logan, R.; O'Brien, K.
- Gene, Vol. 116, Issue 1
Enzymatic properties of cellulases from Humicola insolens
journal, September 1997
- Schülein, Martin
- Journal of Biotechnology, Vol. 57, Issue 1-3, p. 71-81
Cellulosomes: microbial nanomachines that display plasticity in quaternary structure: Cohesin dockerin recognition
journal, March 2007
- Gilbert, Harry J.
- Molecular Microbiology, Vol. 63, Issue 6
Chemical Analyses of Wasp-Associated Streptomyces Bacteria Reveal a Prolific Potential for Natural Products Discovery
journal, February 2011
- Poulsen, Michael; Oh, Dong-Chan; Clardy, Jon
- PLoS ONE, Vol. 6, Issue 2
Regulation of secondary metabolism in streptomycetes
journal, April 2005
- Bibb, Mervyn J.
- Current Opinion in Microbiology, Vol. 8, Issue 2
Microtermolides A and B from Termite-Associated Streptomyces sp. and Structural Revision of Vinylamycin
journal, May 2012
- Carr, Gavin; Poulsen, Michael; Klassen, Jonathan L.
- Organic Letters, Vol. 14, Issue 11
The complex extracellular biology of Streptomyces
journal, March 2010
- Chater, Keith F.; Biró, Sandor; Lee, Kye Joon
- FEMS Microbiology Reviews, Vol. 34, Issue 2
Transcriptional Regulation of Biomass-degrading Enzymes in the Filamentous Fungus Trichoderma reesei
journal, June 2003
- Foreman, Pamela K.; Brown, Doug; Dankmeyer, Lydia
- Journal of Biological Chemistry, Vol. 278, Issue 34, p. 31988-31997
Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes
journal, March 2006
- Janssen, P. H.
- Applied and Environmental Microbiology, Vol. 72, Issue 3
Taxonomic and functional diversity of Streptomyces in a forest soil
journal, April 2013
- Bontemps, Cyril; Toussaint, Maxime; Revol, Pierre-Vincent
- FEMS Microbiology Letters, Vol. 342, Issue 2
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005
- Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C.
- FEMS Microbiology Reviews, Vol. 29, Issue 4
Rapid evolutionary innovation during an Archaean genetic expansion
journal, December 2010
- David, Lawrence A.; Alm, Eric J.
- Nature, Vol. 469, Issue 7328
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Cleavage of cellulose by a CBM33 protein
journal, August 2011
- Forsberg, Zarah; Vaaje-Kolstad, Gustav; Westereng, Bjørge
- Protein Science, Vol. 20, Issue 9
Streptomycin, a Substance Exhibiting Antibiotic Activity Against Gram-Positive and Gram-Negative Bacteria.*
journal, January 1944
- Schatz, A.; Bugle, E.; Waksman, S. A.
- Experimental Biology and Medicine, Vol. 55, Issue 1
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012
- Floudas, Dimitrios; Binder, Manfred; Riley, Robert
- Science, Vol. 336, Issue 6089
Microbial composition alters the response of litter decomposition to environmental change
journal, January 2015
- Matulich, Kristin L.; Martiny, Jennifer B. H.
- Ecology, Vol. 96, Issue 1
Microbial diversity of cellulose hydrolysis
journal, June 2011
- Wilson, David B.
- Current Opinion in Microbiology, Vol. 14, Issue 3
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015
- Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
- Nature Genetics, Vol. 47, Issue 4
Bacterial Protection of Beetle-Fungus Mutualism
journal, October 2008
- Scott, J. J.; Oh, D. -C.; Yuceer, M. C.
- Science, Vol. 322, Issue 5898
Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959
- Miller, G. L.
- Analytical Chemistry, Vol. 31, Issue 3
Microbial communities and their relevance for ecosystem models: Decomposition as a case study
journal, April 2010
- McGuire, Krista L.; Treseder, Kathleen K.
- Soil Biology and Biochemistry, Vol. 42, Issue 4
Targeted gene inactivation in Clostridium phytofermentans shows that cellulose degradation requires the family 9 hydrolase Cphy3367: Clostridium phytofermentans hydrolase genetics
journal, December 2009
- Tolonen, Andrew C.; Chilaka, Amanda C.; Church, George M.
- Molecular Microbiology, Vol. 74, Issue 6
Characterization and Cloning of CelR, a Transcriptional Regulator of Cellulase Genes from Thermomonospora fusca
journal, May 1999
- Spiridonov, Nikolay A.; Wilson, David B.
- Journal of Biological Chemistry, Vol. 274, Issue 19
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
Fungal secretomes—nature’s toolbox for white biotechnology
journal, July 2008
- Bouws, Henning; Wattenberg, Andreas; Zorn, Holger
- Applied Microbiology and Biotechnology, Vol. 80, Issue 3
Gene expression in Pseudomonas aeruginosa biofilms
journal, October 2001
- Whiteley, Marvin; Bangera, M. Gita; Bumgarner, Roger E.
- Nature, Vol. 413, Issue 6858
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012
- Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
- Systematic Biology, Vol. 61, Issue 3
MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004
- Edgar, R. C.
- Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases
journal, May 2014
- Forsberg, Z.; Mackenzie, A. K.; Sorlie, M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 23
Plant Cell Wall Deconstruction by Ascomycete Fungi
journal, September 2013
- Glass, N. Louise; Schmoll, Monika; Cate, Jamie H. D.
- Annual Review of Microbiology, Vol. 67, Issue 1
Biology and biotechnology of Trichoderma
journal, May 2010
- Schuster, André; Schmoll, Monika
- Applied Microbiology and Biotechnology, Vol. 87, Issue 3
Characterization of Actinobacteria Associated with Three Ant–Plant Mutualisms
journal, August 2014
- Hanshew, Alissa S.; McDonald, Bradon R.; Díaz Díaz, Carol
- Microbial Ecology, Vol. 69, Issue 1
Cellulose Degradation by Polysaccharide Monooxygenases
journal, June 2015
- Beeson, William T.; Vu, Van V.; Span, Elise A.
- Annual Review of Biochemistry, Vol. 84, Issue 1
Nitrogen regulator GlnR controls uptake and utilization of non-phosphotransferase-system carbon sources in actinomycetes
journal, December 2015
- Liao, Cheng-Heng; Yao, Lili; Xu, Ya
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 51
Characterization of the Binding Protein-Dependent Cellobiose and Cellotriose Transport System of the Cellulose Degrader Streptomyces reticuli
journal, June 1999
- Schlösser, Andreas; Jantos, Jens; Hackmann, Karl
- Applied and Environmental Microbiology, Vol. 65, Issue 6
Ammonia Fiber Explosion Treatment of Corn Stover
book, January 2004
- Teymouri, Farzaneh; Laureano-Pérez, Lizbeth; Alizadeh, Hasan
- Proceedings of the Twenty-Fifth Symposium on Biotechnology for Fuels and Chemicals Held May 4–7, 2003, in Breckenridge, CO
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins
journal, March 2021
- Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E.
- The ISME Journal, Vol. 15, Issue 8
Comparative mitochondrial genome analysis reveals intron dynamics and gene rearrangements in two Trametes species
journal, January 2021
- Chen, Cheng; Li, Qiang; Fu, Rongtao
- Scientific Reports, Vol. 11, Issue 1
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
text, January 2014
- Stamatakis, A.
- Karlsruhe
Cellulases and their interaction with cellulose
journal, September 1994
- Henrissat, Bernard
- Cellulose, Vol. 1, Issue 3
The synthesis of theStreptomyces reticuli cellulase (Avicelase) is regulated by both activation and repression mechanisms
journal, May 1996
- Walter, S.; Schrempf, H.
- Molecular and General Genetics MGG, Vol. 251, Issue 2
Characterization of Actinobacteria Associated with Three Ant–Plant Mutualisms
journal, August 2014
- Hanshew, Alissa S.; McDonald, Bradon R.; Díaz Díaz, Carol
- Microbial Ecology, Vol. 69, Issue 1
Fungal secretomes—nature’s toolbox for white biotechnology
journal, July 2008
- Bouws, Henning; Wattenberg, Andreas; Zorn, Holger
- Applied Microbiology and Biotechnology, Vol. 80, Issue 3
Biology and biotechnology of Trichoderma
journal, May 2010
- Schuster, André; Schmoll, Monika
- Applied Microbiology and Biotechnology, Vol. 87, Issue 3
Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp.
journal, July 1992
- Bierman, M.; Logan, R.; O'Brien, K.
- Gene, Vol. 116, Issue 1
Production and characterization of multiple cellulolytic enzymes by isolated Streptomyces sp. MDS
journal, December 2012
- Saratale, Ganesh D.; Saratale, Rijuta G.; Oh, Sang Eun
- Biomass and Bioenergy, Vol. 47
Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005
- Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C.
- FEMS Microbiology Reviews, Vol. 29, Issue 4
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences
journal, February 2016
- Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae
- Journal of Molecular Biology, Vol. 428, Issue 4
Regulation of secondary metabolism in streptomycetes
journal, April 2005
- Bibb, Mervyn J.
- Current Opinion in Microbiology, Vol. 8, Issue 2
Microbial diversity of cellulose hydrolysis
journal, June 2011
- Wilson, David B.
- Current Opinion in Microbiology, Vol. 14, Issue 3
Microtermolides A and B from Termite-Associated Streptomyces sp. and Structural Revision of Vinylamycin
journal, May 2012
- Carr, Gavin; Poulsen, Michael; Klassen, Jonathan L.
- Organic Letters, Vol. 14, Issue 11
Gene expression in Pseudomonas aeruginosa biofilms
journal, October 2001
- Whiteley, Marvin; Bangera, M. Gita; Bumgarner, Roger E.
- Nature, Vol. 413, Issue 6858
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists
journal, February 2015
- Kohler, Annegret; Kuo, Alan; Nagy, Laszlo G.
- Nature Genetics, Vol. 47, Issue 4
Continuous evolution of base editors with expanded target compatibility and improved activity
journal, July 2019
- Thuronyi, Benjamin W.; Koblan, Luke W.; Levy, Jonathan M.
- Nature Biotechnology, Vol. 37, Issue 9
Full-length transcriptome analysis of multiple organs and identification of adaptive genes and pathways in Mikania micrantha
journal, February 2022
- Ruan, Xiaoxian; Wang, Zhen; Su, Yingjuan
- Scientific Reports, Vol. 12, Issue 1
Aerobic deconstruction of cellulosic biomass by an insect-associated Streptomyces
journal, January 2013
- Takasuka, Taichi E.; Book, Adam J.; Lewin, Gina R.
- Scientific Reports, Vol. 3, Issue 1
The biosyntheticgene cluster of zorbamycin, a member of the bleomycin family of antitumor antibiotics, from Streptomyces flavoviridis ATCC 21892
journal, January 2009
- Galm, Ute; Wendt-Pienkowski, Evelyn; Wang, Liyan
- Mol. BioSyst., Vol. 5, Issue 1
Estimating divergence times in large molecular phylogenies
journal, November 2012
- Tamura, K.; Battistuzzi, F. U.; Billing-Ross, P.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 47
Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases
journal, May 2014
- Forsberg, Z.; Mackenzie, A. K.; Sorlie, M.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 23
Nitrogen regulator GlnR controls uptake and utilization of non-phosphotransferase-system carbon sources in actinomycetes
journal, December 2015
- Liao, Cheng-Heng; Yao, Lili; Xu, Ya
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 51
Characterization and Cloning of CelR, a Transcriptional Regulator of Cellulase Genes from Thermomonospora fusca
journal, May 1999
- Spiridonov, Nikolay A.; Wilson, David B.
- Journal of Biological Chemistry, Vol. 274, Issue 19
PAML: a program package for phylogenetic analysis by maximum likelihood
journal, January 1997
- Yang, Ziheng
- Bioinformatics, Vol. 13, Issue 5
MEME: discovering and analyzing DNA and protein sequence motifs
journal, July 2006
- Bailey, T. L.; Williams, N.; Misleh, C.
- Nucleic Acids Research, Vol. 34, Issue Web Server
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space
journal, February 2012
- Ronquist, Fredrik; Teslenko, Maxim; van der Mark, Paul
- Systematic Biology, Vol. 61, Issue 3
Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria
journal, January 2001
- Chen, Junqin; Weimer, Paul J.
- Microbiology, Vol. 147, Issue 1
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
Taxonomic and functional diversity of Streptomyces in a forest soil
journal, April 2013
- Bontemps, Cyril; Toussaint, Maxime; Revol, Pierre-Vincent
- FEMS Microbiology Letters, Vol. 342, Issue 2
The complex extracellular biology of Streptomyces
journal, March 2010
- Chater, Keith F.; Biró, Sandor; Lee, Kye Joon
- FEMS Microbiology Reviews, Vol. 34, Issue 2
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007
- Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
- Science, Vol. 315, Issue 5813, p. 804-807
Bacterial Protection of Beetle-Fungus Mutualism
journal, October 2008
- Scott, J. J.; Oh, D. -C.; Yuceer, M. C.
- Science, Vol. 322, Issue 5898
An Oxidative Enzyme Boosting the Enzymatic Conversion of Recalcitrant Polysaccharides
journal, October 2010
- Vaaje-Kolstad, Gustav; Westereng, Bjørge; Horn, Svein J.
- Science, Vol. 330, Issue 6001, p. 219-222
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes
journal, June 2012
- Floudas, Dimitrios; Binder, Manfred; Riley, Robert
- Science, Vol. 336, Issue 6089
Mountain Pine Beetles Colonizing Historical and Naïve Host Trees Are Associated with a Bacterial Community Highly Enriched in Genes Contributing to Terpene Metabolism
journal, March 2013
- Adams, Aaron S.; Aylward, Frank O.; Adams, Sandye M.
- Applied and Environmental Microbiology, Vol. 79, Issue 11
Cellulolytic Streptomyces Strains Associated with Herbivorous Insects Share a Phylogenetically Linked Capacity To Degrade Lignocellulose
journal, May 2014
- Book, Adam J.; Lewin, Gina R.; McDonald, Bradon R.
- Applied and Environmental Microbiology, Vol. 80, Issue 15
Identification of Mycelium-Associated Cellulase from Streptomyces reticuli
journal, January 1989
- Wachinger, Gisela; Bronnenmeier, Karin; Staudenbauer, Walter L.
- Applied and Environmental Microbiology, Vol. 55, Issue 10
CebR as a Master Regulator for Cellulose/Cellooligosaccharide Catabolism Affects Morphological Development in Streptomyces griseus
journal, July 2009
- Marushima, K.; Ohnishi, Y.; Horinouchi, S.
- Journal of Bacteriology, Vol. 191, Issue 19
Microbial Cellulose Utilization: Fundamentals and Biotechnology
journal, September 2002
- Lynd, L. R.; Weimer, P. J.; van Zyl, W. H.
- Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3, p. 506-577
Cellulose Degradation by Polysaccharide Monooxygenases
journal, June 2015
- Beeson, William T.; Vu, Van V.; Span, Elise A.
- Annual Review of Biochemistry, Vol. 84, Issue 1
Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes
journal, April 2011
- Pullan, Steven T.; Chandra, Govind; Bibb, Mervyn J.
- BMC Genomics, Vol. 12, Issue 1
Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi
journal, January 2013
- Zhao, Zhongtao; Liu, Huiquan; Wang, Chenfang
- BMC Genomics, Vol. 14, Issue 1
Comparative genomics of actinomycetes with a focus on natural product biosynthetic genes
journal, January 2013
- Doroghazi, James R.; Metcalf, William W.
- BMC Genomics, Vol. 14, Issue 1
Genome-wide distribution of histone trimethylation reveals a global impact of bisphenol A on telomeric binding proteins and histone acetyltransferase factors: a pilot study with human and in vitro data
journal, December 2022
- D’Cruz, Shereen Cynthia; Hao, Chunxiang; Labussiere, Martin
- Clinical Epigenetics, Vol. 14, Issue 1
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Accounting For Alignment Uncertainty in Phylogenomics
journal, January 2012
- Wu, Martin; Chatterji, Sourav; Eisen, Jonathan A.
- PLoS ONE, Vol. 7, Issue 1
Genomics of Aerobic Cellulose Utilization Systems in Actinobacteria
journal, June 2012
- Anderson, Iain; Abt, Birte; Lykidis, Athanasios
- PLoS ONE, Vol. 7, Issue 6
Ammonia Fiber Explosion Treatment of Corn Stover
journal, January 2004
- Teymouri, Farzaneh; Laureano-Pérez, Lizbeth; Alizadeh, Hasan
- Applied Biochemistry and Biotechnology, Vol. 115, Issue 1-3
Geographic Variation in Bacterial Communities Associated With the Red Turpentine Beetle (Coleoptera: Curculionidae)
journal, April 2010
- Adams, Aaron S.; Adams, Sandye M.; Currie, Cameron R.
- Environmental Entomology, Vol. 39, Issue 2
Microbial composition alters the response of litter decomposition to environmental change
journal, January 2015
- Matulich, Kristin L.; Martiny, Jennifer B. H.
- Ecology, Vol. 96, Issue 1
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
text, January 2014
- Stamatakis, A.
- Karlsruhe
Works referencing / citing this record:
Unraveling the cellulolytic and hemicellulolytic potential of two novel Streptomyces strains
journal, September 2018
- de Melo, Ricardo Rodrigues; Tomazetto, Geizecler; Persinoti, Gabriela Felix
- Annals of Microbiology, Vol. 68, Issue 10
The antimicrobial potential of Streptomyces from insect microbiomes
journal, January 2019
- Chevrette, Marc G.; Carlson, Caitlin M.; Ortega, Humberto E.
- Nature Communications, Vol. 10, Issue 1
Antimicrobial Activity of Actinobacteria Isolated From the Guts of Subterranean Termites
journal, September 2016
- Arango, R. A.; Carlson, C. M.; Currie, C. R.
- Environmental Entomology, Vol. 45, Issue 6
The Termite Fecal Nest: A Framework for the Opportunistic Acquisition of Beneficial Soil Streptomyces (Actinomycetales: Streptomycetaceae)
journal, October 2018
- Chouvenc, Thomas; Elliott, Monica L.; Šobotník, Jan
- Environmental Entomology
Evidence for Widespread Associations between Neotropical Hymenopteran Insects and Actinobacteria
journal, October 2017
- Matarrita-Carranza, Bernal; Moreira-Soto, Rolando D.; Murillo-Cruz, Catalina
- Frontiers in Microbiology, Vol. 8
Densities and inhibitory phenotypes among indigenous Streptomyces spp. vary across native and agricultural habitats
journal, October 2019
- Otto-Hanson, L. K.; Kinkel, L. L.
- Microbial Ecology, Vol. 79, Issue 3
Streptomyces spp. in the biocatalysis toolbox
journal, March 2018
- Spasic, Jelena; Mandic, Mina; Djokic, Lidija
- Applied Microbiology and Biotechnology, Vol. 102, Issue 8
Recent advances in understanding Streptomyces
journal, January 2016
- Chater, Keith F.
- F1000Research, Vol. 5
The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering
posted_content, March 2020
- Wang, Hongfang; Liu, Chunlei; Liu, Zhenguo
- BMC Microbiology
Challenges and Advances for Genetic Engineering of Non-model Bacteria and Uses in Consolidated Bioprocessing
journal, October 2017
- Yan, Qiang; Fong, Stephen S.
- Frontiers in Microbiology, Vol. 8
The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering
posted_content, March 2020
- Wang, Hongfang; Liu, Chunlei; Wang, Yin
- BMC Microbiology
The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering
journal, March 2020
- Wang, Hongfang; Liu, Chunlei; Liu, Zhenguo
- BMC Microbiology, Vol. 20, Issue 1
The antimicrobial potential of Streptomyces from insect microbiomes
journal, January 2019
- Chevrette, Marc G.; Carlson, Caitlin M.; Ortega, Humberto E.
- Nature Communications, Vol. 10, Issue 1
Tracking the Subtle Mutations Driving Host Sensing by the Plant Pathogen
Streptomyces scabies
journal, April 2017
- Jourdan, Samuel; Francis, Isolde M.; Deflandre, Benoit
- mSphere, Vol. 2, Issue 2
Role of GntR Family Regulatory GeneSCO1678in Gluconate Metabolism inStreptomyces coelicolorM145
journal, January 2017
- Tsypik, Olga; Makitrynskyy, Roman; Bera, Agnieszka
- BioMed Research International, Vol. 2017
Evidence for Widespread Associations between Neotropical Hymenopteran Insects and Actinobacteria
journal, October 2017
- Matarrita-Carranza, Bernal; Moreira-Soto, Rolando D.; Murillo-Cruz, Catalina
- Frontiers in Microbiology, Vol. 8
Challenges and Advances for Genetic Engineering of Non-model Bacteria and Uses in Consolidated Bioprocessing
journal, October 2017
- Yan, Qiang; Fong, Stephen S.
- Frontiers in Microbiology, Vol. 8