Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil

Wilhelm, Roland C.; Pepe-Ranney, Charles; Weisenhorn, Pamela; Lipton, Mary; Buckley, Daniel H.

doi:10.1128/mbio.03099-20

Title: Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil

Journal Article · Tue Jan 05 00:00:00 EST 2021 · mBio

DOI:https://doi.org/10.1128/mbio.03099-20· OSTI ID:1863899

^[1];

^[2];

^[3];

^[1]

Cornell Univ., Ithaca, NY (United States)
Argonne National Lab. (ANL), Lemont, IL (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Microorganisms that degrade cellulose utilize extracellular reactions that yield free by-products which can promote interactions with noncellulolytic organisms. We hypothesized that these interactions determine the ecological and physiological traits governing the fate of cellulosic carbon (C) in soil. We performed comparative genomics with genome bins from a shotgun metagenomic-stable isotope probing experiment to characterize the attributes of cellulolytic and noncellulolytic taxa accessing ¹³C from cellulose. We hypothesized that cellulolytic taxa would exhibit competitive traits that limit access, while noncellulolytic taxa would display greater metabolic dependency, such as signatures of adaptive gene loss. We tested our hypotheses by evaluating genomic traits indicative of competitive exclusion or metabolic dependency, such as antibiotic production, growth rate, surface attachment, biomass degrading potential, and auxotrophy. The most ¹³C-enriched taxa were cellulolytic Cellvibrio (Gammaproteobacteria) and Chaetomium (Ascomycota), which exhibited a strategy of self-sufficiency (prototrophy), rapid growth, and competitive exclusion via antibiotic production. Auxotrophy was more prevalent in cellulolytic Actinobacteria than in cellulolytic Proteobacteria, demonstrating differences in dependency among cellulose degraders. Noncellulolytic taxa that accessed ¹³C from cellulose (Planctomycetales, Verrucomicrobia, and Vampirovibrionales) were also more dependent, as indicated by patterns of auxotrophy and ¹³C labeling (i.e., partial labeling or labeling at later stages). Major ¹³C-labeled cellulolytic microbes (e.g., Sorangium, Actinomycetales, Rhizobiales, and Caulobacteraceae) possessed adaptations for surface colonization (e.g., gliding motility, hyphae, attachment structures) signifying the importance of surface ecology in decomposing particulate organic matter. Our results demonstrated that access to cellulosic C was accompanied by ecological trade-offs characterized by differing degrees of metabolic dependency and competitive exclusion.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Cornell Univ., Ithaca, NY (United States)

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

Grant/Contract Number:: SC0016364; SC0004486

OSTI ID:: 1863899

Journal Information:: mBio, Vol. 12, Issue 1; ISSN 2161-2129

Publisher:: American Society for Microbiology (ASM)Copyright Statement

Country of Publication:: United States

Language:: English

References (115)

Assessing fungal contributions to cellulose degradation in soil by using high-throughput stable isotope probing Koechli, Chantal; Campbell, Ashley N.; Pepe-Ranney, Charles Soil Biology and Biochemistry, Vol. 130 https://doi.org/10.1016/j.soilbio.2018.12.013	journal	March 2019
Energy Constraints on the Evolution of Gene Expression Wagner, Andreas Molecular Biology and Evolution, Vol. 22, Issue 6 https://doi.org/10.1093/molbev/msi126	journal	March 2005
QUAST: quality assessment tool for genome assemblies Gurevich, Alexey; Saveliev, Vladislav; Vyahhi, Nikolay Bioinformatics, Vol. 29, Issue 8 https://doi.org/10.1093/bioinformatics/btt086	journal	February 2013
The Arbuscular Mycorrhizal Fungus Funneliformis mosseae Alters Bacterial Communities in Subtropical Forest Soils during Litter Decomposition Gui, Heng; Purahong, Witoon; Hyde, Kevin D. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01120	journal	June 2017
Electronmicroscopic Observations on the Degradation of Cellulose Fibres by Cellvibrio fulvus and Sporocytophaga myxococcoides Berg, B.; Hofsten, B. v.; Pettersson, G. Journal of Applied Bacteriology, Vol. 35, Issue 2 https://doi.org/10.1111/j.1365-2672.1972.tb03692.x	journal	June 1972
Intra-genomic variation in G + C content and its implications for DNA stable isotope probing: DNA-SIP and intra-genomic variation in G + C content Youngblut, Nicholas D.; Buckley, Daniel H. Environmental Microbiology Reports, Vol. 6, Issue 6 https://doi.org/10.1111/1758-2229.12201	journal	October 2014
Temporal Dynamics of Soil Microbial Communities below the Seedbed under Two Contrasting Tillage Regimes Degrune, Florine; Theodorakopoulos, Nicolas; Colinet, Gilles Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01127	journal	June 2017
Proteomic analysis of the Caulobacter crescentus stalk indicates competence for nutrient uptake Ireland, Marcia M. E.; Karty, Jonathan A.; Quardokus, Ellen M. Molecular Microbiology, Vol. 45, Issue 4 https://doi.org/10.1046/j.1365-2958.2002.03071.x	journal	August 2002
Sphingomonas gei sp. nov., isolated from roots of Geum aleppicum Zhu, Lingfang; Si, Meiru; Li, Changfu International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue Pt_4 https://doi.org/10.1099/ijs.0.000074	journal	April 2015
A Rhizobiales-Specific Unipolar Polysaccharide Adhesin Contributes to Rhodopseudomonas palustris Biofilm Formation across Diverse Photoheterotrophic Conditions Fritts, Ryan K.; LaSarre, Breah; Stoner, Ari M. Applied and Environmental Microbiology, Vol. 83, Issue 4 https://doi.org/10.1128/AEM.03035-16	journal	December 2016
Carbohydrate Binding Modules: Biochemical Properties and Novel Applications Shoseyov, O.; Shani, Z.; Levy, I. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2 https://doi.org/10.1128/MMBR.00028-05	journal	June 2006
Unravelling Soil Fungal Communities from Different Mediterranean Land-Use Backgrounds Orgiazzi, Alberto; Lumini, Erica; Nilsson, R. Henrik PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0034847	journal	April 2012
Agricultural Management and Labile Carbon Additions Affect Soil Microbial Community Structure and Interact with Carbon and Nitrogen Cycling Berthrong, Sean T.; Buckley, Daniel H.; Drinkwater, Laurie E. Microbial Ecology, Vol. 66, Issue 1 https://doi.org/10.1007/s00248-013-0225-0	journal	April 2013
Improved Assemblies Using a Source-Agnostic Pipeline for MetaGenomic Assembly by Merging (MeGAMerge) of Contigs Scholz, Matthew; Lo, Chien-Chi; Chain, Patrick S. G. Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep06480	journal	October 2014
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss Morris, J. Jeffrey; Lenski, Richard E.; Zinser, Erik R. mBio, Vol. 3, Issue 2 https://doi.org/10.1128/mBio.00036-12	journal	March 2012
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy Wang, Q.; Garrity, G. M.; Tiedje, J. M. Applied and Environmental Microbiology, Vol. 73, Issue 16 https://doi.org/10.1128/AEM.00062-07	journal	June 2007
Mechanism of cellulose synthesis in Agrobacterium tumefaciens. Matthysse, A. G.; Thomas, D. L.; White, A. R. Journal of Bacteriology, Vol. 177, Issue 4 https://doi.org/10.1128/jb.177.4.1076-1081.1995	journal	February 1995
Functional Redundancy Supports Biodiversity and Ecosystem Function in a Closed and Constant Environment Wohl, Debra L.; Arora, Satyam; Gladstone, Jessica R. Ecology, Vol. 85, Issue 6 https://doi.org/10.1890/03-3050	journal	June 2004
Optimization of cold-active CMCase production by psychrotrophic Sphingomonas sp. FLX-7 from the cold region of China Li, Dapeng; Feng, Lu; Liu, Keran Cellulose, Vol. 23, Issue 2 https://doi.org/10.1007/s10570-016-0859-4	journal	January 2016
Biodiversity characterization of cellulolytic bacteria present on native Chaco soil by comparison of ribosomal RNA genes Talia, Paola; Sede, Silvana M.; Campos, Eleonora Research in Microbiology, Vol. 163, Issue 3 https://doi.org/10.1016/j.resmic.2011.12.001	journal	April 2012
Insight into Dominant Cellulolytic Bacteria from Two Biogas Digesters and Their Glycoside Hydrolase Genes Wei, Yongjun; Zhou, Haokui; Zhang, Jun PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0129921	journal	June 2015
HTSSIP: An R package for analysis of high throughput sequencing data from nucleic acid stable isotope probing (SIP) experiments Youngblut, Nicholas D.; Barnett, Samuel E.; Buckley, Daniel H. PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0189616	journal	January 2018
MEROPS: the database of proteolytic enzymes, their substrates and inhibitors Rawlings, N. D.; Barrett, A. J.; Bateman, A. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr987	journal	November 2011
Asticcacaulis solisilvae sp. nov., isolated from forest soil Kim, Seil; Gong, Gyeongtaek; Park, Tai Hyun International Journal of Systematic and Evolutionary Microbiology, Vol. 63, Issue Pt_10 https://doi.org/10.1099/ijs.0.047423-0	journal	October 2013
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
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics Cantarel, B. L.; Coutinho, P. M.; Rancurel, C. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn663	journal	January 2009
Flavobacterium johnsoniae RemA Is a Mobile Cell Surface Lectin Involved in Gliding Shrivastava, Abhishek; Rhodes, Ryan G.; Pochiraju, Soumya Journal of Bacteriology, Vol. 194, Issue 14 https://doi.org/10.1128/JB.00588-12	journal	July 2012
A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes—Factors affecting enzymes, conversion and synergy Van Dyk, J. S.; Pletschke, B. I. Biotechnology Advances, Vol. 30, Issue 6 https://doi.org/10.1016/j.biotechadv.2012.03.002	journal	November 2012
The COG database: a tool for genome-scale analysis of protein functions and evolution Tatusov, R. L. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.33	journal	January 2000
Planctomycetes and macroalgae, a striking association Lage, Olga M.; Bondoso, Joana Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00267	journal	June 2014
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
Genome reduction in an abundant and ubiquitous soil bacterium ‘Candidatus Udaeobacter copiosus’ Brewer, Tess E.; Handley, Kim M.; Carini, Paul Nature Microbiology, Vol. 2, Issue 2 https://doi.org/10.1038/nmicrobiol.2016.198	journal	October 2016
Physiological interactions between a mesophilic cellulolytic Clostridium and a non-cellulolytic bacterium Cavedon, Katherine; Canale-Parola, Ercole FEMS Microbiology Letters, Vol. 86, Issue 3 https://doi.org/10.1111/j.1574-6968.1992.tb04815.x	journal	February 1992
Nonpareil: a redundancy-based approach to assess the level of coverage in metagenomic datasets Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. Bioinformatics, Vol. 30, Issue 5 https://doi.org/10.1093/bioinformatics/btt584	journal	October 2013
Ecophysiology of Freshwater Verrucomicrobia Inferred from Metagenome-Assembled Genomes He, Shaomei; Stevens, Sarah L. R.; Chan, Leong-Keat mSphere, Vol. 2, Issue 5 https://doi.org/10.1128/mSphere.00277-17	journal	September 2017
Competition Between Ruminal Cellulolytic Bacteria for Adhesion to Cellulose Mosoni, Pascale; Fonty, Gerard; Gouet, Philippe Current Microbiology, Vol. 35, Issue 1 https://doi.org/10.1007/s002849900209	journal	July 1997
SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB Pruesse, E.; Quast, C.; Knittel, K. Nucleic Acids Research, Vol. 35, Issue 21 https://doi.org/10.1093/nar/gkm864	journal	November 2007
On the maverick Planctomycetes Wiegand, Sandra; Jogler, Mareike; Jogler, Christian FEMS Microbiology Reviews, Vol. 42, Issue 6 https://doi.org/10.1093/femsre/fuy029	journal	July 2018
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities Schloss, P. D.; Westcott, S. L.; Ryabin, T. Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541 https://doi.org/10.1128/AEM.01541-09	journal	October 2009
Interactions of Bacteria and Fungi on Decomposing Litter: Differential Extracellular Enzyme Activities Romaní, Anna M.; Fischer, Helmut; Mille-Lindblom, Cecilia Ecology, Vol. 87, Issue 10 https://doi.org/10.1890/0012-9658(2006)87[2559:IOBAFO]2.0.CO;2	journal	October 2006
Cooperation and spatial self-organization determine rate and efficiency of particulate organic matter degradation in marine bacteria Ebrahimi, Ali; Schwartzman, Julia; Cordero, Otto X. Proceedings of the National Academy of Sciences, Vol. 116, Issue 46 https://doi.org/10.1073/pnas.1908512116	journal	October 2019
Selfish, sharing and scavenging bacteria in the Atlantic Ocean: a biogeographical study of bacterial substrate utilisation Reintjes, Greta; Arnosti, Carol; Fuchs, B. The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-018-0326-3	journal	December 2018
Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen: Metabolic response of soil cellulose degraders Schellenberger, Stefanie; Kolb, Steffen; Drake, Harold L. Environmental Microbiology, Vol. 12, Issue 4 https://doi.org/10.1111/j.1462-2920.2009.02128.x	journal	December 2009
Back from the dead; the curious tale of the predatory cyanobacterium Vampirovibrio chlorellavorus Soo, Rochelle M.; Woodcroft, Ben J.; Parks, Donovan H. PeerJ, Vol. 3 https://doi.org/10.7717/peerj.968	journal	January 2015
Infernal 1.1: 100-fold faster RNA homology searches Nawrocki, E. P.; Eddy, S. R. Bioinformatics, Vol. 29, Issue 22 https://doi.org/10.1093/bioinformatics/btt509	journal	September 2013
Characterization of a Planctomycetal Organelle: a Novel Bacterial Microcompartment for the Aerobic Degradation of Plant Saccharides Erbilgin, Onur; McDonald, Kent L.; Kerfeld, Cheryl A. Applied and Environmental Microbiology, Vol. 80, Issue 7 https://doi.org/10.1128/AEM.03887-13	journal	January 2014
Wood decay under the microscope Schwarze, Francis W. M. R. Fungal Biology Reviews, Vol. 21, Issue 4 https://doi.org/10.1016/j.fbr.2007.09.001	journal	November 2007
MATAM: reconstruction of phylogenetic marker genes from short sequencing reads in metagenomes Pericard, Pierre; Dufresne, Yoann; Couderc, Loïc Bioinformatics, Vol. 34, Issue 4 https://doi.org/10.1093/bioinformatics/btx644	journal	October 2017
Versatile and open software for comparing large genomes Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L. Genome Biology, Vol. 5, Issue 2, R12 https://doi.org/10.1186/gb-2004-5-2-r12	journal	January 2004
Identification of a 349-Kilodalton Protein (Gli349) Responsible for Cytadherence and Glass Binding during Gliding of Mycoplasma mobile Uenoyama, Atsuko; Kusumoto, Akiko; Miyata, Makoto Journal of Bacteriology, Vol. 186, Issue 5 https://doi.org/10.1128/jb.186.5.1537-1545.2004	journal	March 2004
Complete genome sequence of the myxobacterium Sorangium cellulosum Schneiker, Susanne; Perlova, Olena; Kaiser, Olaf Nature Biotechnology, Vol. 25, Issue 11 https://doi.org/10.1038/nbt1354	journal	October 2007
Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces Robledo, M.; Rivera, L.; Jiménez-Zurdo, Jose I. Microbial Cell Factories, Vol. 11, Issue 1 https://doi.org/10.1186/1475-2859-11-125	journal	January 2012
High-throughput generation, optimization and analysis of genome-scale metabolic models Henry, Christopher S.; DeJongh, Matthew; Best, Aaron A. Nature Biotechnology, Vol. 28, Issue 9 https://doi.org/10.1038/nbt.1672	journal	August 2010
Plant Carbohydrate Scavenging through TonB-Dependent Receptors: A Feature Shared by Phytopathogenic and Aquatic Bacteria Blanvillain, Servane; Meyer, Damien; Boulanger, Alice PLoS ONE, Vol. 2, Issue 2 https://doi.org/10.1371/journal.pone.0000224	journal	February 2007
The Development of Media Suitable for the Microorganisms Morphologically Resembling Planctomyces spp., Pirellula spp., and other Planctomycetales from Various Aquatic Habitats Using Dilute Media Schlesner, Heinz Systematic and Applied Microbiology, Vol. 17, Issue 1 https://doi.org/10.1016/S0723-2020(11)80042-1	journal	March 1994
Metagenome-Wide Association Study and Machine Learning Prediction of Bulk Soil Microbiome and Crop Productivity Chang, Hao-Xun; Haudenshield, James S.; Bowen, Charles R. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00519	journal	April 2017
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
Biodegradation of cellulosic and lignocellulosic waste by Pseudoxanthomonas sp R-28 Kumar, Mohit; Revathi, K.; Khanna, Sunil Carbohydrate Polymers, Vol. 134 https://doi.org/10.1016/j.carbpol.2015.08.072	journal	December 2015
The mysterious nature of bacterial surface (gliding) motility: A focal adhesion-based mechanism in Myxococcus xanthus Islam, Salim T.; Mignot, Tâm Seminars in Cell & Developmental Biology, Vol. 46 https://doi.org/10.1016/j.semcdb.2015.10.033	journal	October 2015
From genome mining to phenotypic microarrays: Planctomycetes as source for novel bioactive molecules Jeske, Olga; Jogler, Mareike; Petersen, Jörn Antonie van Leeuwenhoek, Vol. 104, Issue 4 https://doi.org/10.1007/s10482-013-0007-1	journal	August 2013
Broad-spectrum antibiotic resistance of Planctomycetes organisms determined by Etest Cayrou, C.; Raoult, D.; Drancourt, M. Journal of Antimicrobial Chemotherapy, Vol. 65, Issue 10 https://doi.org/10.1093/jac/dkq290	journal	August 2010
Simulating metagenomic stable isotope probing datasets with MetaSIPSim Barnett, Samuel E.; Buckley, Daniel H. BMC Bioinformatics, Vol. 21, Issue 1 https://doi.org/10.1186/s12859-020-3372-6	journal	January 2020
Multisubstrate Isotope Labeling and Metagenomic Analysis of Active Soil Bacterial Communities Verastegui, Y.; Cheng, J.; Engel, K. mBio, Vol. 5, Issue 4 https://doi.org/10.1128/mBio.01157-14	journal	July 2014
Syntrophic metabolism of a co-culture containing Clostridium cellulolyticum and Rhodopseudomonas palustris for hydrogen production Jiao, Yongqin; Navid, Ali; Stewart, Benjamin J. International Journal of Hydrogen Energy, Vol. 37, Issue 16 https://doi.org/10.1016/j.ijhydene.2012.05.100	journal	August 2012
MEGAN Community Edition - Interactive Exploration and Analysis of Large-Scale Microbiome Sequencing Data Huson, Daniel H.; Beier, Sina; Flade, Isabell PLOS Computational Biology, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pcbi.1004957	journal	June 2016
Characterizing the Key Agents in a Disease-Suppressed Soil Managed by Reductive Soil Disinfestation Liu, Liangliang; Huang, Xinqi; Zhao, Jun Applied and Environmental Microbiology, Vol. 85, Issue 7 https://doi.org/10.1128/AEM.02992-18	journal	April 2019
Cellulose degradation by one mesophilic strain Caulobacter sp. FMC1 under both aerobic and anaerobic conditions Song, Na; Cai, Hai-Yuan; Yan, Zai-Sheng Bioresource Technology, Vol. 131 https://doi.org/10.1016/j.biortech.2013.01.003	journal	March 2013
Explaining microbial genomic diversity in light of evolutionary ecology Cordero, Otto X.; Polz, Martin F. Nature Reviews Microbiology, Vol. 12, Issue 4 https://doi.org/10.1038/nrmicro3218	journal	March 2014
The use of kapok fibres for enrichment cultures of lignocellulose-degrading bacteria Nilsson, Thomas; Björdal, Charlotte International Biodeterioration & Biodegradation, Vol. 61, Issue 1 https://doi.org/10.1016/j.ibiod.2007.06.009	journal	January 2008
Microbial Volatiles: Small Molecules with an Important Role in Intra- and Inter-Kingdom Interactions Schulz-Bohm, Kristin; Martín-Sánchez, Lara; Garbeva, Paolina Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02484	journal	December 2017
Cloning, sequencing and overexpression of a Sinorhizobium meliloti M5N1CS carboxymethyl-cellulase gene P., Michaud; A., Belaich; B., Courtois Applied Microbiology and Biotechnology, Vol. 58, Issue 6 https://doi.org/10.1007/s00253-002-0953-4	journal	May 2002
Phylogenetic conservatism of functional traits in microorganisms Martiny, Adam C.; Treseder, Kathleen; Pusch, Gordon The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.160	journal	December 2012
Bacteriocinogenic Activity in the Genus Cellvibrio Halliwell, G.; Sweet, C. Journal of General Microbiology, Vol. 77, Issue 2 https://doi.org/10.1099/00221287-77-2-363	journal	August 1973
The Systemic Imprint of Growth and Its Uses in Ecological (Meta)Genomics Vieira-Silva, Sara; Rocha, Eduardo P. C. PLoS Genetics, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pgen.1000808	journal	January 2010
Efficacy of Chaetomium Species as Biological Control Agents against Phytophthora nicotianae Root Rot in Citrus Hung, Phung Manh; Wattanachai, Pongnak; Kasem, Soytong Mycobiology, Vol. 43, Issue 3 https://doi.org/10.5941/MYCO.2015.43.3.288	journal	September 2015
Reshaping Data with the reshape Package Wickham, Hadley Journal of Statistical Software, Vol. 21, Issue 12 https://doi.org/10.18637/jss.v021.i12	journal	January 2007
Modular Assembly of Polysaccharide-Degrading Marine Microbial Communities Enke, Tim N.; Datta, Manoshi S.; Schwartzman, Julia Current Biology, Vol. 29, Issue 9 https://doi.org/10.1016/j.cub.2019.03.047	journal	May 2019
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Effective cellulose degradation by a mixed-culture system composed of a cellulolytic Clostridium and aerobic non-cellulolytic bacteria Kato, Souichiro; Haruta, Shin; Cui, Zong Jun FEMS Microbiology Ecology, Vol. 51, Issue 1 https://doi.org/10.1016/j.femsec.2004.07.015	journal	December 2004
Diversity of Glycosyl Hydrolases from Cellulose-Depleting Communities Enriched from Casts of Two Earthworm Species Beloqui, A.; Nechitaylo, T. Y.; Lopez-Cortes, N. Applied and Environmental Microbiology, Vol. 76, Issue 17 https://doi.org/10.1128/AEM.00902-10	journal	July 2010
Identification of a 521-Kilodalton Protein (Gli521) Involved in Force Generation or Force Transmission for Mycoplasma mobile Gliding Seto, Shintaro; Uenoyama, Atsuko; Miyata, Makoto Journal of Bacteriology, Vol. 187, Issue 10 https://doi.org/10.1128/JB.187.10.3502-3510.2005	journal	May 2005
KBase: The United States Department of Energy Systems Biology Knowledgebase Arkin, Adam P.; Cottingham, Robert W.; Henry, Christopher S. Nature Biotechnology, Vol. 36, Issue 7 https://doi.org/10.1038/nbt.4163	journal	July 2018
Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers Štursová, Martina; Žifčáková, Lucia; Leigh, Mary Beth FEMS Microbiology Ecology, Vol. 80, Issue 3 https://doi.org/10.1111/j.1574-6941.2012.01343.x	journal	March 2012
Cellulosomes: plant-cell-wall-degrading enzyme complexes Doi, Roy H.; Kosugi, Akihiko Nature Reviews Microbiology, Vol. 2, Issue 7 https://doi.org/10.1038/nrmicro925	journal	July 2004
Long-Term Enrichment of Stress-Tolerant Cellulolytic Soil Populations following Timber Harvesting Evidenced by Multi-Omic Stable Isotope Probing Wilhelm, Roland C.; Cardenas, Erick; Leung, Hilary Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00537	journal	April 2017
Long-term no-till: A major driver of fungal communities in dryland wheat cropping systems Sharma-Poudyal, Dipak; Schlatter, Daniel; Yin, Chuntao PLOS ONE, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pone.0184611	journal	September 2017
The contentious nature of soil organic matter Lehmann, Johannes; Kleber, Markus Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature16069	journal	November 2015
Adherence of Clostridium thermocellum to cellulose. Bayer, E. A.; Kenig, R.; Lamed, R. Journal of Bacteriology, Vol. 156, Issue 2 https://doi.org/10.1128/JB.156.2.818-827.1983	journal	January 1983
Resource Partitioning between Bacteria, Fungi, and Protists in the Detritusphere of an Agricultural Soil Kramer, Susanne; Dibbern, Dörte; Moll, Julia Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01524	journal	September 2016
Universality of priming effect: An analysis using thirty five soils with contrasted properties sampled from five continents Perveen, Nazia; Barot, Sébastien; Maire, Vincent Soil Biology and Biochemistry, Vol. 134 https://doi.org/10.1016/j.soilbio.2019.03.027	journal	July 2019
Competition for cellobiose among three predominant ruminal cellulolytic bacteria under substrate-excess and substrate-limited conditions Shi, Y.; Weimer, P. J. Applied and Environmental Microbiology, Vol. 63, Issue 2 https://doi.org/10.1128/AEM.63.2.743-748.1997	journal	February 1997
Helical flow of surface protein required for bacterial gliding motility Nakane, Daisuke; Sato, Keiko; Wada, Hirofumi Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1219753110	journal	June 2013
Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil: Impact of white-rot fungi on bacteria colonizing wood Folman, Larissa B.; Klein Gunnewiek, Paulien J. A.; Boddy, Lynne FEMS Microbiology Ecology, Vol. 63, Issue 2 https://doi.org/10.1111/j.1574-6941.2007.00425.x	journal	February 2008
Vibrio cholerae filamentation promotes chitin surface attachment at the expense of competition in biofilms Wucher, Benjamin R.; Bartlett, Thomas M.; Hoyos, Mona Proceedings of the National Academy of Sciences, Vol. 116, Issue 28 https://doi.org/10.1073/pnas.1819016116	journal	June 2019
Universal and species-specific bacterial ‘fungiphiles’ in the mycospheres of different basidiomycetous fungi Warmink, J. A.; Nazir, R.; van Elsas, J. D. Environmental Microbiology, Vol. 11, Issue 2 https://doi.org/10.1111/j.1462-2920.2008.01767.x	journal	February 2009
Characterization of a Symbiotic Coculture of Clostridium thermohydrosulfuricum YM3 and Clostridium thermocellum YM4 Mori, Yutaka Applied and Environmental Microbiology, Vol. 56, Issue 1 https://doi.org/10.1128/AEM.56.1.37-42.1990	journal	January 1990
Cellobiose dehydrogenase formation by filamentous fungus Chaetomium sp. INBI 2-26(−) Vasil’chenko, L. G.; Khromonygina, V. V.; Karapetyan, K. N. Journal of Biotechnology, Vol. 119, Issue 1 https://doi.org/10.1016/j.jbiotec.2005.03.023	journal	September 2005
Devosia soli sp. nov., isolated from greenhouse soil in Korea Yoo, S. -H.; Weon, H. -Y.; Kim, B. -Y. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 11 https://doi.org/10.1099/ijs.0.64214-0	journal	November 2006
Cellulolytic Bacteria Associated with the Gut of Dendroctonus armandi Larvae (Coleoptera: Curculionidae: Scolytinae) Hu, Xia; Yu, Jiamin; Wang, Chunyan Forests, Vol. 5, Issue 3 https://doi.org/10.3390/f5030455	journal	March 2014
Occurrence of novel verrucomicrobial species, endosymbiotic and associated with parthenogenesis in Xiphinema americanum-group species (Nematoda, Longidoridae). Vandekerckhove, T. T.; Willems, A.; Gillis, M. International Journal of Systematic and Evolutionary Microbiology, Vol. 50, Issue 6 https://doi.org/10.1099/00207713-50-6-2197	journal	November 2000
Evolution of High Cellulolytic Activity in Symbiotic Streptomyces through Selection of Expanded Gene Content and Coordinated Gene Expression Book, Adam J.; Lewin, Gina R.; McDonald, Bradon R. PLOS Biology, Vol. 14, Issue 6 https://doi.org/10.1371/journal.pbio.1002475	journal	June 2016
Reclassification and emended description of Caulobacter leidyi as Sphingomonas leidyi comb. nov., and emendation of the genus Sphingomonas Chen, H.; Jogler, M.; Rohde, M. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue Pt 12 https://doi.org/10.1099/ijs.0.039636-0	journal	January 2012
The antiSMASH database, a comprehensive database of microbial secondary metabolite biosynthetic gene clusters Blin, Kai; Medema, Marnix H.; Kottmann, Renzo Nucleic Acids Research, Vol. 45, Issue D1 https://doi.org/10.1093/nar/gkw960	journal	October 2016
Identification of Cellulose-Responsive Bacterial and Fungal Communities in Geographically and Edaphically Different Soils by Using Stable Isotope Probing Eichorst, Stephanie A.; Kuske, Cheryl R. Applied and Environmental Microbiology, Vol. 78, Issue 7 https://doi.org/10.1128/AEM.07313-11	journal	January 2012
Bacterial contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing Wilhelm, Roland C.; Singh, Rahul; Eltis, Lindsay D. The ISME Journal, Vol. 13, Issue 2 https://doi.org/10.1038/s41396-018-0279-6	journal	September 2018
Identification of cellulolytic bacteria in soil by stable isotope probing el Zahar Haichar, Feth; Achouak, Wafa; Christen, Richard Environmental Microbiology, Vol. 9, Issue 3 https://doi.org/10.1111/j.1462-2920.2006.01182.x	journal	March 2007
Tracking microbial colonization in fecal microbiota transplantation experiments via genome-resolved metagenomics Lee, Sonny T. M.; Kahn, Stacy A.; Delmont, Tom O. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0270-x	journal	May 2017
Unearthing the Ecology of Soil Microorganisms Using a High Resolution DNA-SIP Approach to Explore Cellulose and Xylose Metabolism in Soil Pepe-Ranney, Charles; Campbell, Ashley N.; Koechli, Chantal N. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00703	journal	May 2016
Draft Genome Sequence of Herpetosiphon geysericola GC-42, a Nonphototrophic Member of the Chloroflexi Class Chloroflexia Ward, Lewis M.; Hemp, James; Pace, Laura A. Genome Announcements, Vol. 3, Issue 6 https://doi.org/10.1128/genomeA.01352-15	journal	November 2015
Ethanol Production by Thermophilic Bacteria: Fermentation of Cellulosic Substrates by Cocultures of Clostridium thermocellum and Clostridium thermohydrosulfuricum Ng, Thomas K.; Ben-Bassat, Arie; Zeikus, J. G. Applied and Environmental Microbiology, Vol. 41, Issue 6 https://doi.org/10.1128/AEM.41.6.1337-1343.1981	journal	January 1981
Auxotrophy and intrapopulation complementary in the ‘interactome’ of a cultivated freshwater model community Garcia, Sarahi L.; Buck, Moritz; McMahon, Katherine D. Molecular Ecology, Vol. 24, Issue 17 https://doi.org/10.1111/mec.13319	journal	August 2015
Evolutionary Systems Biology of Amino Acid Biosynthetic Cost in Yeast Barton, Michael D.; Delneri, Daniela; Oliver, Stephen G. PLoS ONE, Vol. 5, Issue 8 https://doi.org/10.1371/journal.pone.0011935	journal	August 2010
Stable-Isotope Probing Identifies Uncultured Planctomycetes as Primary Degraders of a Complex Heteropolysaccharide in Soil Wang, Xiaoqing; Sharp, Christine E.; Jones, Gareth M. Applied and Environmental Microbiology, Vol. 81, Issue 14 https://doi.org/10.1128/AEM.00055-15	journal	May 2015

Similar Records

Microbial food web mapping: linking carbon cycling and community structure in soils through pyrosequencing enabled stable isotope probing

Technical Report · Sun Mar 15 00:00:00 EDT 2015 · OSTI ID:1863899

Buckley, Daniel

MaxBin: an automated binning method to recover individual genomes from metagenomes using an expectation-maximization algorithm

Journal Article · Fri Aug 01 00:00:00 EDT 2014 · Microbiome · OSTI ID:1863899

Wu, Yu-Wei; Tang, Yung-Hsu; Tringe, Susannah G.; +2 more

Long-Term Cellulose Enrichment Selects for Highly Cellulolytic Consortia and Competition for Public Goods

Journal Article · Tue Apr 26 00:00:00 EDT 2022 · mSystems · OSTI ID:1863899

Lewin, Gina R.; Davis, Nicole M.; McDonald, Bradon R.; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
decomposition
ecological trade-offs
metagenomics
stable isotope probing
metaproteomics
metabolic dependency
competitive exclusion
surface ecology
soil carbon cycling
ecogenomics

Title: Competitive Exclusion and Metabolic Dependency among Microorganisms Structure the Cellulose Economy of an Agricultural Soil

Citation Formats

References (115)

Similar Records

Related Subjects