Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics

Ziels, Ryan M.; Nobu, Masaru K.; Sousa, Diana Z.

doi:10.1128/msystems.00159-19

Title: Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics

Journal Article · Tue Aug 06 00:00:00 EDT 2019 · mSystems

DOI:https://doi.org/10.1128/msystems.00159-19· OSTI ID:1626172

^[1]; Nobu, Masaru K. ^[2]; Sousa, Diana Z. ^[3]

Univ. of Waterloo, ON (Canada)
National Inst. of Advanced Industrial Science and Technology (AIST), Tsukuba (Japan)
Wageningen Univ. (Netherlands)

Linking the genomic content of uncultivated microbes to their metabolic functions remains a critical challenge in microbial ecology. Resolving this challenge has implications for improving our management of key microbial interactions in biotechnologies such as anaerobic digestion, which relies on slow-growing syntrophic and methanogenic communities to produce renewable methane from organic waste. In this study, we combined DNA stable-isotope probing (SIP) with genome-centric metagenomics to recover the genomes of populations enriched in¹³C after growing on [¹³C]butyrate. Differential abundance analysis of recovered genomic bins across the SIP metagenomes identified two metagenome-assembled genomes (MAGs) that were significantly enriched in heavy [¹³C]DNA. Phylogenomic analysis assigned one MAG to the genus Syntrophomonas and the other MAG to the genus Methanothrix. Metabolic reconstruction of the annotated genomes showed that the Syntrophomonas genome encoded all the enzymes for beta-oxidizing butyrate, as well as several mechanisms for interspecies electron transfer via electron transfer flavoproteins, hydrogenases, and formate dehydrogenases. The Syntrophomonas genome shared low average nucleotide identity (<95%) with any cultured representative species, indicating that it is a novel species that plays a significant role in syntrophic butyrate degradation within anaerobic digesters. The Methanothrix genome contained the complete pathway for acetoclastic methanogenesis, indicating that it was enriched in¹³C from syntrophic acetate transfer. This study demonstrates the potential of stable-isotope-informed genome-resolved metagenomics to identifyin situinterspecies metabolic cooperation within syntrophic consortia important to anaerobic waste treatment as well as global carbon cycling.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Sciences and Engineering Research Council of Canada (NSERC); USEPA; Netherlands Organization for Scientific Research (NWO); Wageningen Institute for Environmental and Climate Research (WIMEK)

Grant/Contract Number:: AC02-05CH11231; RD835567; 323009; 040.15.014

OSTI ID:: 1626172

Journal Information:: mSystems, Vol. 4, Issue 4; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 14 works

Citation information provided by
Web of Science

References (92)

Flavin-Based Electron Bifurcation, Ferredoxin, Flavodoxin, and Anaerobic Respiration With Protons (Ech) or NAD+ (Rnf) as Electron Acceptors: A Historical Review Buckel, Wolfgang; Thauer, Rudolf K. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00401	journal	March 2018
Description of a New Strain of Methanothrix soehngenii and Rejection of Methanothrix concilii as a Synonym of Methanothrix soehngenii Touzel, J. P.; Prensier, G.; Roustan, J. L. International Journal of Systematic Bacteriology, Vol. 38, Issue 1 https://doi.org/10.1099/00207713-38-1-30	journal	January 1988
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
Characterization and nutritional properties of Methanothrix concilii sp. nov., a mesophilic, aceticlastic methanogen Patel, G. B. Canadian Journal of Microbiology, Vol. 30, Issue 11 https://doi.org/10.1139/m84-221	journal	November 1984
Carbon Monoxide, Hydrogen, and Formate Metabolism during Methanogenesis from Acetate by Thermophilic Cultures of Methanosarcina and Methanothrix Strains Zinder, S. H.; Anguish, T. Applied and Environmental Microbiology, Vol. 58, Issue 10 https://doi.org/10.1128/aem.58.10.3323-3329.1992	journal	January 1992
Membrane-Bound Electron Transport in Methanosaeta thermophila Welte, C.; Deppenmeier, U. Journal of Bacteriology, Vol. 193, Issue 11 https://doi.org/10.1128/JB.00162-11	journal	April 2011
Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and Genome Analyzer systems Minoche, André E.; Dohm, Juliane C.; Himmelbauer, Heinz Genome Biology, Vol. 12, Issue 11 https://doi.org/10.1186/gb-2011-12-11-r112	journal	January 2011
Identification of Surprisingly Diverse Type IV Pili, across a Broad Range of Gram-Positive Bacteria Imam, Saheed; Chen, Zhongqiang; Roos, David S. PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028919	journal	December 2011
The genome of Syntrophus aciditrophicus: Life at the thermodynamic limit of microbial growth McInerney, M. J.; Rohlin, L.; Mouttaki, H. Proceedings of the National Academy of Sciences, Vol. 104, Issue 18 https://doi.org/10.1073/pnas.0610456104	journal	April 2007
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
Long-chain fatty acids inhibition and adaptation process in anaerobic thermophilic digestion: Batch tests, microbial community structure and mathematical modelling Palatsi, J.; Illa, J.; Prenafeta-Boldú, F. X. Bioresource Technology, Vol. 101, Issue 7 https://doi.org/10.1016/j.biortech.2009.11.069	journal	April 2010
Tepidanaerobacter acetatoxydans sp. nov., an anaerobic, syntrophic acetate-oxidizing bacterium isolated from two ammonium-enriched mesophilic methanogenic processes Westerholm, Maria; Roos, Stefan; Schnürer, Anna Systematic and Applied Microbiology, Vol. 34, Issue 4 https://doi.org/10.1016/j.syapm.2010.11.018	journal	June 2011
Fatty Acid-Oxidizing Consortia along a Nutrient Gradient in the Florida Everglades Chauhan, Ashvini; Ogram, Andrew Applied and Environmental Microbiology, Vol. 72, Issue 4 https://doi.org/10.1128/AEM.72.4.2400-2406.2006	journal	April 2006
Genomic Insights into Syntrophy: The Paradigm for Anaerobic Metabolic Cooperation Sieber, Jessica R.; McInerney, Michael J.; Gunsalus, Robert P. Annual Review of Microbiology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-micro-090110-102844	journal	October 2012
MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data Vallenet, David; Belda, Eugeni; Calteau, Alexandra Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1194	journal	November 2012
Succession of endophytic fungi and arbuscular mycorrhizal fungi associated with the growth of plant and their correlation with secondary metabolites in the roots of plants Dang, Hanli; Zhang, Tao; Wang, Zhongke BMC Plant Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s12870-021-02942-6	journal	April 2021
Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology Karp, P. D.; Paley, S. M.; Krummenacker, M. Briefings in Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1093/bib/bbp043	journal	December 2009
Diversity and dynamics of microbial communities in engineered environments and their implications for process stability Briones, Aurelio; Raskin, Lutgarde Current Opinion in Biotechnology, Vol. 14, Issue 3 https://doi.org/10.1016/S0958-1669(03)00065-X	journal	June 2003
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
DNA stable-isotope probing Neufeld, Josh D.; Vohra, Jyotsna; Dumont, Marc G. Nature Protocols, Vol. 2, Issue 4 https://doi.org/10.1038/nprot.2007.109	journal	April 2007
DNA-SIP based genome-centric metagenomics identifies key long-chain fatty acid-degrading populations in anaerobic digesters with different feeding frequencies Ziels, Ryan M.; Sousa, Diana Z.; Stensel, H. David The ISME Journal, Vol. 12, Issue 1 https://doi.org/10.1038/ismej.2017.143	journal	September 2017
BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae Journal of Molecular Biology, Vol. 428, Issue 4 https://doi.org/10.1016/j.jmb.2015.11.006	journal	February 2016
Annotation data for 13-C enriched MAGs from DNA SIP with anaerobic butyrate degrading microcosms Ziels, Ryan figshare https://doi.org/10.6084/m9.figshare.7761710	dataset	January 2019
The Genome Characteristics and Predicted Function of Methyl-Group Oxidation Pathway in the Obligate Aceticlastic Methanogens, Methanosaeta spp Zhu, Jinxing; Zheng, Huajun; Ai, Guomin PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0036756	journal	May 2012
Monitoring the dynamics of syntrophic β-oxidizing bacteria during anaerobic degradation of oleic acid by quantitative PCR Ziels, Ryan M.; Beck, David A. C.; Martí, Magalí FEMS Microbiology Ecology, Vol. 91, Issue 4 https://doi.org/10.1093/femsec/fiv028	journal	March 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
Datura genome reveals duplications of psychoactive alkaloid biosynthetic genes and high mutation rate following tissue culture Rajewski, Alex; Carter-House, Derreck; Stajich, Jason BMC Genomics, Vol. 22, Issue 1 https://doi.org/10.1186/s12864-021-07489-2	journal	March 2021
Long-chain fatty acid feeding frequency in anaerobic codigestion impacts syntrophic community structure and biokinetics Ziels, Ryan M.; Beck, David A. C.; Stensel, H. David Water Research, Vol. 117 https://doi.org/10.1016/j.watres.2017.03.060	journal	June 2017
A Proteomic View at the Biochemistry of Syntrophic Butyrate Oxidation in Syntrophomonas wolfei Schmidt, Alexander; Müller, Nicolai; Schink, Bernhard PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0056905	journal	February 2013
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
Evolution under Fluctuating Environments Explains Observed Robustness in Metabolic Networks Soyer, Orkun S.; Pfeiffer, Thomas PLoS Computational Biology, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pcbi.1000907	journal	August 2010
MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices Li, Dinghua; Luo, Ruibang; Liu, Chi-Man Methods, Vol. 102 https://doi.org/10.1016/j.ymeth.2016.02.020	journal	June 2016
UGA is an additional glycine codon in uncultured SR1 bacteria from the human microbiota Campbell, J. H.; O'Donoghue, P.; Campbell, A. G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 14, p. 5540-5545 https://doi.org/10.1073/pnas.1303090110	journal	March 2013
The genome of S yntrophorhabdus aromaticivorans strain UI provides new insights for syntrophic aromatic compound metabolism and electron flow Nobu, Masaru K.; Narihiro, Takashi; Hideyuki, Tamaki Environmental Microbiology, Vol. 17, Issue 12 https://doi.org/10.1111/1462-2920.12444	journal	March 2014
Direct Exchange of Electrons Within Aggregates of an Evolved Syntrophic Coculture of Anaerobic Bacteria Summers, Z. M.; Fogarty, H. E.; Leang, C. Science, Vol. 330, Issue 6009, p. 1413-1415 https://doi.org/10.1126/science.1196526	journal	December 2010
Effect of dilution rate on the microbial structure of a mesophilic butyrate-degrading methanogenic community during continuous cultivation Tang, Yue-Qin; Shigematsu, Toru; Morimura, Shigeru Applied Microbiology and Biotechnology, Vol. 75, Issue 2 https://doi.org/10.1007/s00253-006-0819-2	journal	January 2007
The FlxABCD-HdrABC proteins correspond to a novel NADH dehydrogenase/heterodisulfide reductase widespread in anaerobic bacteria and involved in ethanol metabolism in D esulfovibrio vulgaris Hildenborough : Role of FlxABCD-HdrABC in Ramos, Ana Raquel; Grein, Fabian; Oliveira, Gonçalo P. Environmental Microbiology, Vol. 17, Issue 7 https://doi.org/10.1111/1462-2920.12689	journal	January 2015
Extracellular electron transfer via microbial nanowires Reguera, Gemma; McCarthy, Kevin D.; Mehta, Teena Nature, Vol. 435, Issue 7045, p. 1098-1101 https://doi.org/10.1038/nature03661	journal	June 2005
UPARSE: highly accurate OTU sequences from microbial amplicon reads Edgar, Robert C. Nature Methods, Vol. 10, Issue 10 https://doi.org/10.1038/nmeth.2604	journal	August 2013
Metatranscriptomic Evidence for Direct Interspecies Electron Transfer between Geobacter and Methanothrix Species in Methanogenic Rice Paddy Soils Holmes, Dawn E.; Shrestha, Pravin M.; Walker, David J. F. Applied and Environmental Microbiology, Vol. 83, Issue 9 https://doi.org/10.1128/AEM.00223-17	journal	March 2017
A genomic view on syntrophic versus non-syntrophic lifestyle in anaerobic fatty acid degrading communities Worm, Petra; Koehorst, Jasper J.; Visser, Michael Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 12 https://doi.org/10.1016/j.bbabio.2014.06.005	journal	December 2014
Functional bacterial and archaeal community structures of major trophic groups in a full-scale anaerobic sludge digester Ariesyady, H.; Ito, T.; Okabe, S. Water Research, Vol. 41, Issue 7 https://doi.org/10.1016/j.watres.2006.12.036	journal	April 2007
The Electron Bifurcating FixABCX Protein Complex from Azotobacter vinelandii : Generation of Low-Potential Reducing Equivalents for Nitrogenase Catalysis Ledbetter, Rhesa N.; Garcia Costas, Amaya M.; Lubner, Carolyn E. Biochemistry, Vol. 56, Issue 32 https://doi.org/10.1021/acs.biochem.7b00389	journal	August 2017
A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane Rotaru, Amelia-Elena; Shrestha, Pravin Malla; Liu, Fanghua Energy Environ. Sci., Vol. 7, Issue 1 https://doi.org/10.1039/C3EE42189A	journal	January 2014
Syntrophomonadaceae-Affiliated Species as Active Butyrate-Utilizing Syntrophs in Paddy Field Soil Liu, Pengfei; Qiu, Qiongfen; Lu, Yahai Applied and Environmental Microbiology, Vol. 77, Issue 11 https://doi.org/10.1128/AEM.00190-11	journal	April 2011
Genome-centric resolution of microbial diversity, metabolism and interactions in anaerobic digestion: Genome-centric resolution through deep metagenomics Vanwonterghem, Inka; Jensen, Paul D.; Rabaey, Korneel Environmental Microbiology, Vol. 18, Issue 9 https://doi.org/10.1111/1462-2920.13382	journal	July 2016
Binning metagenomic contigs by coverage and composition Alneberg, Johannes; Bjarnason, Brynjar Smári; de Bruijn, Ino Nature Methods, Vol. 11, Issue 11 https://doi.org/10.1038/nmeth.3103	journal	September 2014
Kinetics of Butyrate, Acetate, and Hydrogen Metabolism in a Thermophilic, Anaerobic, Butyrate-Degrading Triculture Ahring, Birgitte K.; Westermann, Peter Applied and Environmental Microbiology, Vol. 53, Issue 2 https://doi.org/10.1128/aem.53.2.434-439.1987	journal	February 1987
Ecophysiology of syntrophic communities that degrade saturated and unsaturated long-chain fatty acids: Ecophysiology of syntrophic LCFA degradation Sousa, Diana Z.; Smidt, Hauke; Alves, Maria M. FEMS Microbiology Ecology, Vol. 68, Issue 3 https://doi.org/10.1111/j.1574-6941.2009.00680.x	journal	June 2009
Deeper insight into the structure of the anaerobic digestion microbial community; the biogas microbiome database is expanded with 157 new genomes Treu, Laura; Kougias, Panagiotis G.; Campanaro, Stefano Bioresource Technology, Vol. 216 https://doi.org/10.1016/j.biortech.2016.05.081	journal	September 2016
A Generalized Method for Thermodynamic State Analysis of Environmental Systems Kleerebezem, Robbert; Van Loosdrecht, Mark C. M. Critical Reviews in Environmental Science and Technology, Vol. 40, Issue 1 https://doi.org/10.1080/10643380802000974	journal	January 2010
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Peat: home to novel syntrophic species that feed acetate- and hydrogen-scavenging methanogens Schmidt, Oliver; Hink, Linda; Horn, Marcus A. The ISME Journal, Vol. 10, Issue 8 https://doi.org/10.1038/ismej.2015.256	journal	January 2016
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Energetics of syntrophic cooperation in methanogenic degradation Schink, B. Microbiology and Molecular Biology Reviews, Vol. 61, Issue 2 https://doi.org/10.1128/mmbr.61.2.262-280.1997	journal	June 1997
Who eats what, where and when? Isotope-labelling experiments are coming of age Neufeld, Josh D.; Wagner, Michael; Murrell, J. Colin The ISME Journal, Vol. 1, Issue 2 https://doi.org/10.1038/ismej.2007.30	journal	May 2007
Culture-Independent Analyses Reveal Novel Anaerolineaceae as Abundant Primary Fermenters in Anaerobic Digesters Treating Waste Activated Sludge McIlroy, Simon J.; Kirkegaard, Rasmus H.; Dueholm, Morten S. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01134	journal	June 2017
The genome of Syntrophomonas wolfei: new insights into syntrophic metabolism and biohydrogen production: Syntrophomonas wolfei genome Sieber, Jessica R.; Sims, David R.; Han, Cliff Environmental Microbiology https://doi.org/10.1111/j.1462-2920.2010.02237.x	journal	June 2010
Microbial nanowires for bioenergy applications Malvankar, Nikhil S.; Lovley, Derek R. Current Opinion in Biotechnology, Vol. 27 https://doi.org/10.1016/j.copbio.2013.12.003	journal	June 2014
The role of anaerobic digestion in the emerging energy economy Batstone, Damien John; Virdis, Bernardino Current Opinion in Biotechnology, Vol. 27 https://doi.org/10.1016/j.copbio.2014.01.013	journal	June 2014
Variation among Desulfovibrio Species in Electron Transfer Systems Used for Syntrophic Growth Meyer, B.; Kuehl, J.; Deutschbauer, A. M. Journal of Bacteriology, Vol. 195, Issue 5 https://doi.org/10.1128/JB.01959-12	journal	December 2012
Quantitative detection of previously characterized syntrophic bacteria in anaerobic wastewater treatment systems by sequence-specific rRNA cleavage method Narihiro, Takashi; Terada, Takeshi; Ohashi, Akiko Water Research, Vol. 46, Issue 7 https://doi.org/10.1016/j.watres.2012.01.034	journal	May 2012
Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life Parks, Donovan H.; Rinke, Christian; Chuvochina, Maria Nature Microbiology, Vol. 2, Issue 11 https://doi.org/10.1038/s41564-017-0012-7	journal	September 2017
Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option Walker, David J. F.; Nevin, Kelly P.; Holmes, Dawn E. The ISME Journal, Vol. 14, Issue 3 https://doi.org/10.1038/s41396-019-0575-9	journal	January 2020
Syntrophomonas zehnderi sp. nov., an anaerobe that degrades long-chain fatty acids in co-culture with Methanobacterium formicicum Sousa, D. Z.; Smidt, H.; Alves, M. M. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 3 https://doi.org/10.1099/ijs.0.64734-0	journal	March 2007
Methanothrix soehngenii gen. nov. sp. nov., a new acetotrophic non-hydrogen-oxidizing methane bacterium Huser, Beat A.; Wuhrmann, Karl; Zehnder, Alexander J. B. Archives of Microbiology, Vol. 132, Issue 1 https://doi.org/10.1007/BF00690808	journal	July 1982
Genome fasta files for 13-C enriched genomes from DNA-SIP with anaerobic butyrate degrading microcosms Ziels, Ryan figshare https://doi.org/10.6084/m9.figshare.7761776.v1	dataset	January 2019
The Iron-Hydrogenase of Thermotoga maritima Utilizes Ferredoxin and NADH Synergistically: a New Perspective on Anaerobic Hydrogen Production Schut, G. J.; Adams, M. W. W. Journal of Bacteriology, Vol. 191, Issue 13 https://doi.org/10.1128/JB.01582-08	journal	May 2009
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
Insights into the phylogeny and coding potential of microbial dark matter Rinke, Christian; Schwientek, Patrick; Sczyrba, Alexander Nature, Vol. 499, Issue 7459 https://doi.org/10.1038/nature12352	journal	July 2013
FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix Price, M. N.; Dehal, P. S.; Arkin, A. P. Molecular Biology and Evolution, Vol. 26, Issue 7 https://doi.org/10.1093/molbev/msp077	journal	April 2009
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
Ferroferric oxide triggered possible direct interspecies electron transfer between Syntrophomonas and Methanosaeta to enhance waste activated sludge anaerobic digestion Zhao, Zisheng; Li, Yang; Yu, Qilin Bioresource Technology, Vol. 250 https://doi.org/10.1016/j.biortech.2017.11.003	journal	February 2018
Communities stimulated with ethanol to perform direct interspecies electron transfer for syntrophic metabolism of propionate and butyrate Zhao, Zhiqiang; Zhang, Yaobin; Yu, Qilin Water Research, Vol. 102 https://doi.org/10.1016/j.watres.2016.07.005	journal	October 2016
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
Membrane Complexes of Syntrophomonas wolfei Involved in Syntrophic Butyrate Degradation and Hydrogen Formation Crable, Bryan R.; Sieber, Jessica R.; Mao, Xinwei Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01795	journal	November 2016
DNA–DNA hybridization values and their relationship to whole-genome sequence similarities Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1 https://doi.org/10.1099/ijs.0.64483-0	journal	January 2007
A Filtering Method to Generate High Quality Short Reads Using Illumina Paired-End Technology Eren, A. Murat; Vineis, Joseph H.; Morrison, Hilary G. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066643	journal	June 2013
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
Bacterial species may exist, metagenomics reveal: Bacterial species may exist Caro-Quintero, Alejandro; Konstantinidis, Konstantinos T. Environmental Microbiology, Vol. 14, Issue 2 https://doi.org/10.1111/j.1462-2920.2011.02668.x	journal	December 2011
The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism: Importance of interspecies hydrogen and formate transfer Sieber, Jessica R.; Le, Huynh M.; McInerney, Michael J. Environmental Microbiology, Vol. 16, Issue 1 https://doi.org/10.1111/1462-2920.12269	journal	October 2013
Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei Sieber, Jessica R.; Crable, Bryan R.; Sheik, Cody S. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00115	journal	February 2015
Anaerobic co-digestion of landfill leachate and acid mine drainage using up-flow anaerobic sludge blanket reactor Zhou, Shiqi; Wang, Jin; Peng, Shuchuan Environmental Science and Pollution Research, Vol. 28, Issue 7 https://doi.org/10.1007/s11356-020-11207-y	journal	October 2020
Evidence of reversed electron transport in syntrophic butyrate or benzoate oxidation by Syntrophomonas wolfei and Syntrophus buswellii Wallrabenstein, Christina; Schink, Bernhard Archives of Microbiology, Vol. 162, Issue 1-2 https://doi.org/10.1007/bf00264387	journal	July 1994
Salinimonas marina sp. nov. Isolated from Jeju Island Marine Sediment Kim, Minji; Lee, Ki-Eun; Cha, In-Tae Current Microbiology, Vol. 78, Issue 8 https://doi.org/10.1007/s00284-021-02576-9	journal	June 2021
Sphingopyxis jiangsuensis sp. nov. Isolated From the Surface Water of the Yellow Sea Gao, Zeng-Yu; Xue, Hua-Peng; Wang, Lu Current Microbiology, Vol. 79, Issue 7 https://doi.org/10.1007/s00284-022-02895-5	journal	June 2022
Characterizing the molecular regulation of inhibitory immune checkpoints with multimodal single-cell screens Papalexi, Efthymia; Mimitou, Eleni P.; Butler, Andrew W. Nature Genetics, Vol. 53, Issue 3 https://doi.org/10.1038/s41588-021-00778-2	journal	March 2021
The complete chloroplast genome of Gleditsia sinensis and Gleditsia japonica: genome organization, comparative analysis, and development of taxon specific DNA mini-barcodes Tan, Wei; Gao, Han; Jiang, Weiling Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-73392-7	journal	October 2020
Detection of Active Butyrate-Degrading Microorganisms in Methanogenic Sludges by RNA-Based Stable Isotope Probing Hatamoto, Masashi; Imachi, Hiroyuki; Yashiro, Yuto Applied and Environmental Microbiology, Vol. 74, Issue 11 https://doi.org/10.1128/aem.00045-08	journal	April 2008
Syntrophomonas wolfei Uses an NADH-Dependent, Ferredoxin-Independent [FeFe]-Hydrogenase To Reoxidize NADH Losey, Nathaniel A.; Mus, Florence; Peters, John W. Applied and Environmental Microbiology, Vol. 83, Issue 20 https://doi.org/10.1128/aem.01335-17	journal	August 2017
Involvement of NADH:Acceptor Oxidoreductase and Butyryl Coenzyme A Dehydrogenase in Reversed Electron Transport during Syntrophic Butyrate Oxidation by Syntrophomonas wolfei Muller, N.; Schleheck, D.; Schink, B. Journal of Bacteriology, Vol. 191, Issue 19 https://doi.org/10.1128/jb.01605-08	journal	July 2009
Annotation data for 13-C enriched MAGs from DNA SIP with anaerobic butyrate degrading microcosms Ziels, Ryan figshare https://doi.org/10.6084/m9.figshare.7761710.v1	dataset	January 2019

Similar Records

DNA-SIP based genome-centric metagenomics identifies key long-chain fatty acid-degrading populations in anaerobic digesters with different feeding frequencies

Journal Article · Tue Sep 12 00:00:00 EDT 2017 · The ISME Journal · OSTI ID:1626172

Ziels, Ryan M.; Sousa, Diana Z.; Stensel, H. David; +1 more

Membrane Complexes of Syntrophomonas wolfei Involved in Syntrophic Butyrate Degradation and Hydrogen Formation

Journal Article · Wed Nov 09 00:00:00 EST 2016 · Frontiers in Microbiology · OSTI ID:1626172

Crable, Bryan R.; Sieber, Jessica R.; Mao, Xinwei; +5 more

Catabolism and interactions of uncultured organisms shaped by eco-thermodynamics in methanogenic bioprocesses

Journal Article · Fri Jul 24 00:00:00 EDT 2020 · Microbiome · OSTI ID:1626172

Nobu, Masaru K.; Narihiro, Takashi; Mei, Ran; +5 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
microbiology
anaerobic catabolic pathways
anaerobic digestion
metagenomics
methanogenesis
stable-isotope probing
syntrophy

Title: Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics

Citation Formats

References (92)

Similar Records

Related Subjects