Microbial Community Analysis with Ribosomal Gene Fragments from Shotgun Metagenomes

Guo, Jiarong; Cole, James R.; Zhang, Qingpeng; Brown, C. Titus; Tiedje, James M.

doi:10.1128/AEM.02772-15

Title: Microbial Community Analysis with Ribosomal Gene Fragments from Shotgun Metagenomes

Journal Article · Fri Oct 16 00:00:00 EDT 2015 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/AEM.02772-15· OSTI ID:1470720

Guo, Jiarong ^[1]; Cole, James R. ^[1]; Zhang, Qingpeng ^[1]; Brown, C. Titus ^[2]; Tiedje, James M. ^[1]

Michigan State Univ., East Lansing, MI (United States)
Michigan State Univ., East Lansing, MI (United States); Univ. of California, Davis, CA (United States)

Shotgun metagenomic sequencing does not depend on gene-targeted primers or PCR amplification; thus, it is not affected by primer bias or chimeras. However, searching rRNA genes from large shotgun Illumina data sets is computationally expensive, and no approach exists for unsupervised community analysis of small-subunit (SSU) rRNA gene fragments retrieved from shotgun data. We present a pipeline, SSUsearch, to achieve the faster identification of short-subunit rRNA gene fragments and enabled unsupervised community analysis with shotgun data. It also includes classification and copy number correction, and the output can be used by traditional amplicon analysis platforms. Shotgun metagenome data using this pipeline yielded higher diversity estimates than amplicon data but retained the grouping of samples in ordination analyses. We applied this pipeline to soil samples with paired shotgun and amplicon data and confirmed bias against Verrucomicrobia in a commonly used V6-V8 primer set, as well as discovering likely bias against Actinobacteria and for Verrucomicrobia in a commonly used V4 primer set. In conclusion, this pipeline can utilize all variable regions in SSU rRNA and also can be applied to large-subunit (LSU) rRNA genes for confirmation of community structure.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

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

Grant/Contract Number:: SC0004601

OSTI ID:: 1470720

Journal Information:: Applied and Environmental Microbiology, Vol. 82, Issue 1; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 42 works

Citation information provided by
Web of Science

References (63)

Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Lane, D. J.; Pace, B.; Olsen, G. J. Proceedings of the National Academy of Sciences, Vol. 82, Issue 20 https://doi.org/10.1073/pnas.82.20.6955	journal	October 1985
Metagenomics – the key to the uncultured microbes Streit, Wolfgang R.; Schmitz, Ruth A. Current Opinion in Microbiology, Vol. 7, Issue 5 https://doi.org/10.1016/j.mib.2004.08.002	journal	October 2004
Exploring Microbial Diversity and Taxonomy Using SSU rRNA Hypervariable Tag Sequencing Huse, Susan M.; Dethlefsen, Les; Huber, Julie A. PLoS Genetics, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pgen.1000255	journal	November 2008
Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms Caporaso, J. Gregory; Lauber, Christian L.; Walters, William A. The ISME Journal, Vol. 6, Issue 8 https://doi.org/10.1038/ismej.2012.8	journal	March 2012
Microbial diversity in the deep sea and the underexplored "rare biosphere" Sogin, M. L.; Morrison, H. G.; Huber, J. A. Proceedings of the National Academy of Sciences, Vol. 103, Issue 32 https://doi.org/10.1073/pnas.0605127103	journal	July 2006
The Ribosomal Database Project: improved alignments and new tools for rRNA analysis Cole, J. R.; Wang, Q.; Cardenas, E. Nucleic Acids Research, Vol. 37, Issue Database https://doi.org/10.1093/nar/gkn879	journal	January 2009
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
The under-recognized dominance of Verrucomicrobia in soil bacterial communities Bergmann, Gaddy T.; Bates, Scott T.; Eilers, Kathryn G. Soil Biology and Biochemistry, Vol. 43, Issue 7 https://doi.org/10.1016/j.soilbio.2011.03.012	journal	July 2011
Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons Haas, B. J.; Gevers, D.; Earl, A. M. Genome Research, Vol. 21, Issue 3 https://doi.org/10.1101/gr.112730.110	journal	January 2011
Community structure and metabolism through reconstruction of microbial genomes from the environment Tyson, Gene W.; Chapman, Jarrod; Hugenholtz, Philip Nature, Vol. 428, Issue 6978 https://doi.org/10.1038/nature02340	journal	February 2004
A human gut microbial gene catalogue established by metagenomic sequencing Qin, Junjie; Li, Ruiqiang; Raes, Jeroen Nature, Vol. 464, Issue 7285 https://doi.org/10.1038/nature08821	journal	March 2010
Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities: Metagenomic and rRNA diversity characterization Shakya, Migun; Quince, Christopher; Campbell, James H. Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12086	journal	February 2013
Review and re-analysis of domain-specific 16S primers Baker, G. C.; Smith, J. J.; Cowan, D. A. Journal of Microbiological Methods, Vol. 55, Issue 3 https://doi.org/10.1016/j.mimet.2003.08.009	journal	December 2003
Critical Evaluation of Two Primers Commonly Used for Amplification of Bacterial 16S rRNA Genes Frank, J. A.; Reich, C. I.; Sharma, S. Applied and Environmental Microbiology, Vol. 74, Issue 8 https://doi.org/10.1128/AEM.02272-07	journal	February 2008
Identification and removal of ribosomal RNA sequences from metatranscriptomes Schmieder, Robert; Lim, Yan Wei; Edwards, Robert Bioinformatics, Vol. 28, Issue 3 https://doi.org/10.1093/bioinformatics/btr669	journal	December 2011
Identification of ribosomal RNA genes in metagenomic fragments Huang, Ying; Gilna, Paul; Li, Weizhong Bioinformatics, Vol. 25, Issue 10 https://doi.org/10.1093/bioinformatics/btp161	journal	April 2009
rRNASelector: A computer program for selecting ribosomal RNA encoding sequences from metagenomic and metatranscriptomic shotgun libraries Lee, Jae-Hak; Yi, Hana; Chun, Jongsik The Journal of Microbiology, Vol. 49, Issue 4 https://doi.org/10.1007/s12275-011-1213-z	journal	August 2011
Metaxa: a software tool for automated detection and discrimination among ribosomal small subunit (12S/16S/18S) sequences of archaea, bacteria, eukaryotes, mitochondria, and chloroplasts in metagenomes and environmental sequencing datasets Bengtsson, Johan; Eriksson, K. Martin; Hartmann, Martin Antonie van Leeuwenhoek, Vol. 100, Issue 3 https://doi.org/10.1007/s10482-011-9598-6	journal	June 2011
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
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
PhyloSift: phylogenetic analysis of genomes and metagenomes Darling, Aaron E.; Jospin, Guillaume; Lowe, Eric PeerJ, Vol. 2 https://doi.org/10.7717/peerj.243	journal	January 2014
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
MEGAN analysis of metagenomic data Huson, D. H.; Auch, A. F.; Qi, J. Genome Research, Vol. 17, Issue 3 https://doi.org/10.1101/gr.5969107	journal	February 2007
Metagenomic 16S rDNA Illumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities: Using Logares, Ramiro; Sunagawa, Shinichi; Salazar, Guillem Environmental Microbiology, Vol. 16, Issue 9 https://doi.org/10.1111/1462-2920.12250	journal	September 2013
Coverage evaluation of universal bacterial primers using the metagenomic datasets Mao, Dan-Ping; Zhou, Quan; Chen, Chong-Yu BMC Microbiology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2180-12-66	journal	January 2012
Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies Klindworth, Anna; Pruesse, Elmar; Schweer, Timmy Nucleic Acids Research, Vol. 41, Issue 1 https://doi.org/10.1093/nar/gks808	journal	August 2012
Bacterial Communities in the Rhizosphere of Biofuel Crops Grown on Marginal Lands as Evaluated by 16S rRNA Gene Pyrosequences da C. Jesus, Ederson; Susilawati, Endang; Smith, Stephanie L. BioEnergy Research, Vol. 3, Issue 1 https://doi.org/10.1007/s12155-009-9073-7	journal	January 2010
FLASH: fast length adjustment of short reads to improve genome assemblies Magoc, T.; Salzberg, S. L. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr507	journal	September 2011
A High-Throughput DNA Sequence Aligner for Microbial Ecology Studies Schloss, Patrick D. PLoS ONE, Vol. 4, Issue 12 https://doi.org/10.1371/journal.pone.0008230	journal	December 2009
Ribosomal Database Project: data and tools for high throughput rRNA analysis Cole, James R.; Wang, Qiong; Fish, Jordan A. Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1244	journal	November 2013
Efficient algorithms for accurate hierarchical clustering of huge datasets: tackling the entire protein space Loewenstein, Y.; Portugaly, E.; Fromer, M. Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn174	journal	June 2008
Compilation of small ribosomal subunit RNA structures Neefs, Jean-Marc; Van de Peer, Yves; De Rijk, Peter Nucleic Acids Research, Vol. 21, Issue 13 https://doi.org/10.1093/nar/21.13.3025	journal	January 1993
CopyRighter: a rapid tool for improving the accuracy of microbial community profiles through lineage-specific gene copy number correction Angly, Florent E.; Dennis, Paul G.; Skarshewski, Adam Microbiome, Vol. 2, Issue 1 https://doi.org/10.1186/2049-2618-2-11	journal	April 2014
Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB DeSantis, T. Z.; Hugenholtz, P.; Larsen, N. Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5069-5072 https://doi.org/10.1128/AEM.03006-05	journal	July 2006
IPython: A System for Interactive Scientific Computing Perez, Fernando; Granger, Brian E. Computing in Science & Engineering, Vol. 9, Issue 3 https://doi.org/10.1109/MCSE.2007.53	journal	January 2007
Reproducibility and quantitation of amplicon sequencing-based detection Zhou, Jizhong; Wu, Liyou; Deng, Ye The ISME Journal, Vol. 5, Issue 8 https://doi.org/10.1038/ismej.2011.11	journal	February 2011
High-Throughput Metagenomic Technologies for Complex Microbial Community Analysis: Open and Closed Formats Zhou, Jizhong; He, Zhili; Yang, Yunfeng mBio, Vol. 6, Issue 1 https://doi.org/10.1128/mBio.02288-14	journal	January 2015
Defining the core Arabidopsis thaliana root microbiome Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera Nature, Vol. 488, Issue 7409 https://doi.org/10.1038/nature11237	journal	August 2012
Taxonomic Precision of Different Hypervariable Regions of 16S rRNA Gene and Annotation Methods for Functional Bacterial Groups in Biological Wastewater Treatment Guo, Feng; Ju, Feng; Cai, Lin PLoS ONE, Vol. 8, Issue 10 https://doi.org/10.1371/journal.pone.0076185	journal	October 2013
Identifying the Dominant Soil Bacterial Taxa in Libraries of 16S rRNA and 16S rRNA Genes Janssen, P. H. Applied and Environmental Microbiology, Vol. 72, Issue 3 https://doi.org/10.1128/AEM.72.3.1719-1728.2006	journal	March 2006
Metagenomic species profiling using universal phylogenetic marker genes Sunagawa, Shinichi; Mende, Daniel R.; Zeller, Georg Nature Methods, Vol. 10, Issue 12 https://doi.org/10.1038/nmeth.2693	journal	October 2013
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A. Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402 https://doi.org/10.1093/nar/25.17.3389	journal	September 1997
BLAT---The BLAST-Like Alignment Tool Kent, W. J. Genome Research, Vol. 12, Issue 4 https://doi.org/10.1101/gr.229202	journal	March 2002
Soil Microbial Community Responses to a Decade of Warming as Revealed by Comparative Metagenomics Luo, Chengwei; Rodriguez-R, Luis M.; Johnston, Eric R. Applied and Environmental Microbiology, Vol. 80, Issue 5 https://doi.org/10.1128/AEM.03712-13	journal	December 2013
PyNAST: a flexible tool for aligning sequences to a template alignment Caporaso, J. G.; Bittinger, K.; Bushman, F. D. Bioinformatics, Vol. 26, Issue 2 https://doi.org/10.1093/bioinformatics/btp636	journal	November 2009
Short pyrosequencing reads suffice for accurate microbial community analysis Liu, Z.; Lozupone, C.; Hamady, M. Nucleic Acids Research, Vol. 35, Issue 18 https://doi.org/10.1093/nar/gkm541	journal	August 2007
Assessing and Improving Methods Used in Operational Taxonomic Unit-Based Approaches for 16S rRNA Gene Sequence Analysis Schloss, Patrick D.; Westcott, Sarah L. Applied and Environmental Microbiology, Vol. 77, Issue 10 https://doi.org/10.1128/AEM.02810-10	journal	March 2011
PhylOTU: A High-Throughput Procedure Quantifies Microbial Community Diversity and Resolves Novel Taxa from Metagenomic Data Sharpton, Thomas J.; Riesenfeld, Samantha J.; Kembel, Steven W. PLoS Computational Biology, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pcbi.1001061	journal	January 2011
Detection of Actinobacteria cultivated from environmental samples reveals bias in universal primers Farris, M. H.; Olson, J. B. Letters in Applied Microbiology, Vol. 45, Issue 4 https://doi.org/10.1111/j.1472-765X.2007.02198.x	journal	October 2007
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Fungal community analysis by high-throughput sequencing of amplified markers - a user's guide Lindahl, Björn D.; Nilsson, R. Henrik; Tedersoo, Leho New Phytologist, Vol. 199, Issue 1 https://doi.org/10.1111/nph.12243	journal	March 2013
From Genus to Phylum: Large-Subunit and Internal Transcribed Spacer rRNA Operon Regions Show Similar Classification Accuracies Influenced by Database Composition Porras-Alfaro, Andrea; Liu, Kuan-Liang; Kuske, Cheryl R. Applied and Environmental Microbiology, Vol. 80, Issue 3 https://doi.org/10.1128/AEM.02894-13	journal	November 2013
Fungal/bacterial ratios in grasslands with contrasting nitrogen management de Vries, Franciska T.; Hoffland, Ellis; van Eekeren, Nick Soil Biology and Biochemistry, Vol. 38, Issue 8 https://doi.org/10.1016/j.soilbio.2006.01.008	journal	August 2006
Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models Waring, Bonnie G.; Averill, Colin; Hawkes, Christine V. Ecology Letters, Vol. 16, Issue 7 https://doi.org/10.1111/ele.12125	journal	May 2013
Influence of corn, switchgrass, and prairie cropping systems on soil microbial communities in the upper Midwest of the United States Jesus, Ederson da C.; Liang, Chao; Quensen, John F. GCB Bioenergy, Vol. 8, Issue 2 https://doi.org/10.1111/gcbb.12289	journal	December 2015
Divergence and Redundancy of 16S rRNA Sequences in Genomes with Multiple rrn Operons Acinas, S. G.; Marcelino, L. A.; Klepac-Ceraj, V. Journal of Bacteriology, Vol. 186, Issue 9 https://doi.org/10.1128/JB.186.9.2629-2635.2004	journal	April 2004
Microbial community resemblance methods differ in their ability to detect biologically relevant patterns Kuczynski, Justin; Liu, Zongzhi; Lozupone, Catherine Nature Methods, Vol. 7, Issue 10 https://doi.org/10.1038/nmeth.1499	journal	September 2010
Evaluation of 23S rRNA PCR Primers for Use in Phylogenetic Studies of Bacterial Diversity Hunt, Dana E.; Klepac-Ceraj, Vanja; Acinas, Silvia G. Applied and Environmental Microbiology, Vol. 72, Issue 3 https://doi.org/10.1128/AEM.72.3.2221-2225.2006	journal	March 2006
Evaluation of LSU rRNA-gene PCR primers for analysis of arbuscular mycorrhizal fungal communities via terminal restriction fragment length polymorphism analysis Mummey, Daniel L.; Rillig, Matthias C. Journal of Microbiological Methods, Vol. 70, Issue 1 https://doi.org/10.1016/j.mimet.2007.04.002	journal	July 2007
Accurate, Rapid Taxonomic Classification of Fungal Large-Subunit rRNA Genes Liu, Kuan-Liang; Porras-Alfaro, Andrea; Kuske, Cheryl R. Applied and Environmental Microbiology, Vol. 78, Issue 5 https://doi.org/10.1128/AEM.06826-11	journal	December 2011
Factors That Affect Large Subunit Ribosomal DNA Amplicon Sequencing Studies of Fungal Communities: Classification Method, Primer Choice, and Error Porter, Teresita M.; Golding, G. Brian PLoS ONE, Vol. 7, Issue 4 https://doi.org/10.1371/journal.pone.0035749	journal	April 2012
Current state and perspectives of fungal DNA barcoding and rapid identification procedures Begerow, Dominik; Nilsson, Henrik; Unterseher, Martin Applied Microbiology and Biotechnology, Vol. 87, Issue 1 https://doi.org/10.1007/s00253-010-2585-4	journal	April 2010
Comparison of 16S rRNA and protein-coding genes as molecular markers for assessing microbial diversity (Bacteria and Archaea) in ecosystems Roux, Simon; Enault, François; Bronner, Gisè FEMS Microbiology Ecology, Vol. 78, Issue 3 https://doi.org/10.1111/j.1574-6941.2011.01190.x	journal	September 2011

Cited By (12)

Large-scale differences in microbial biodiversity discovery between 16S amplicon and shotgun sequencing Tessler, Michael; Neumann, Johannes S.; Afshinnekoo, Ebrahim Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-06665-3	journal	July 2017
Taxonomy of anaerobic digestion microbiome reveals biases associated with the applied high throughput sequencing strategies Campanaro, Stefano; Treu, Laura; Kougias, Panagiotis G. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-20414-0	journal	January 2018
Soil hydrology drives ecological niche differentiation in a native prairie microbiome Griffin, James S.; Haug, Loren A.; Rivera, Vivien A. FEMS Microbiology Ecology, Vol. 96, Issue 1 https://doi.org/10.1093/femsec/fiz163	journal	October 2019
CaptureSeq: Capture-based enrichment of cpn60 gene fragments empowers pan-Domain profiling of microbial communities without universal PCR Links, Matthew G.; Dumonceaux, Tim J.; McCarthy, Luke https://doi.org/10.1101/492116	preprint	August 2020
Arbuscular mycorrhizal fungi promote coexistence and niche divergence of sympatric palm species on a remote oceanic island Osborne, Owen G.; De-Kayne, Rishi; Bidartondo, Martin I. New Phytologist, Vol. 217, Issue 3 https://doi.org/10.1111/nph.14850	journal	October 2017
High-throughput DNA sequencing technologies for water and wastewater analysis Chan, Alexander WY; Naphtali, James; Schellhorn, Herb E. Science Progress, Vol. 102, Issue 4 https://doi.org/10.1177/0036850419881855	journal	October 2019
Uncovering the trimethylamine-producing bacteria of the human gut microbiota Rath, Silke; Heidrich, Benjamin; Pieper, Dietmar H. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0271-9	journal	May 2017
Verrucomicrobia are prevalent in north-temperate freshwater lakes and display class-level preferences between lake habitats Chiang, Edna; Schmidt, Marian L.; Berry, Michelle A. PLOS ONE, Vol. 13, Issue 3 https://doi.org/10.1371/journal.pone.0195112	journal	March 2018
DNA Sequencing as a Tool to Monitor Marine Ecological Status Goodwin, Kelly D.; Thompson, Luke R.; Duarte, Bernardo Frontiers in Marine Science, Vol. 4 https://doi.org/10.3389/fmars.2017.00107	journal	May 2017
New Biological Insights Into How Deforestation in Amazonia Affects Soil Microbial Communities Using Metagenomics and Metagenome-Assembled Genomes Kroeger, Marie E.; Delmont, Tom O.; Eren, A. M. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01635	journal	July 2018
JGI QC impact on assembly, binning, phylogenomics, and functional analysis Whitham, Jason North Carolina State Univ., Raleigh, NC (United States) https://doi.org/10.25982/62657.1515/1779219	dataset	January 2021
Impact of BBDuk metagenomic read trimming and decontamination Whitham, Jason North Carolina State Univ., Raleigh, NC (United States) https://doi.org/10.25982/77705.1341/1779218	dataset	January 2021

Similar Records

Primer and platform effects on 16S rRNA tag sequencing

Journal Article · Tue Aug 04 00:00:00 EDT 2015 · Frontiers in Microbiology · OSTI ID:1470720

Tremblay, Julien; Singh, Kanwar; Fern, Alison; +7 more

Metagenomics Reveals Pervasive Bacterial Populations and Reduced Community Diversity across the Alaska Tundra Ecosystem

Journal Article · Mon Apr 25 00:00:00 EDT 2016 · Frontiers in Microbiology · OSTI ID:1470720

Johnston, Eric R.; Rodriguez-R, Luis M.; Luo, Chengwei; +8 more

Effects of error, chimera, bias, and GC content on the accuracy of amplicon sequencing

Journal Article · Thu Dec 21 00:00:00 EST 2023 · mSystems · OSTI ID:1470720

Qin, Yujia; Wu, Liyou; Zhang, Qiuting; +7 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: Microbial Community Analysis with Ribosomal Gene Fragments from Shotgun Metagenomes

Citation Formats

References (63)

Cited By (12)

Similar Records

Related Subjects