Unlocking short read sequencing for metagenomics

Rodrigue, Sébastien; Materna, Arne C.; Timberlake, Sonia C.; Blackburn, Matthew C.; Malmstrom, Rex R.; Alm, Eric J.; Chisholm, Sallie W.

doi:10.1371/journal.pone.0011840

Cited by 168Genomics and Phylogenetic StudiesEnvironmental DNA in Biodiversity StudiesMicrobial Community Ecology and Physiology

Unlocking short read sequencing for metagenomics

Open access

Rodrigue, Sébastien, Materna, Arne C., Timberlake, Sonia C., Blackburn, Matthew C., Malmstrom, Rex R., Alm, Eric J., Chisholm, Sallie W.·2010·PLoS ONE

DOI 10.1371/journal.pone.0011840PMC PMC2911387

Open this paper in CoChat — free account Open PDF

Abstract

BACKGROUND: Different high-throughput nucleic acid sequencing platforms are currently available but a trade-off currently exists between the cost and number of reads that can be generated versus the read length that can be achieved. METHODOLOGY/PRINCIPAL FINDINGS: We describe an experimental and computational pipeline yielding millions of reads that can exceed 200 bp with quality scores approaching that of traditional Sanger sequencing. The method combines an automatable gel-less library construction step with paired-end sequencing on a short-read instrument. With appropriately sized library inserts, mate-pair sequences can overlap, and we describe the SHERA software package that joins them to form a longer composite read. CONCLUSIONS/SIGNIFICANCE: This strategy is broadly applicable to sequencing applications that benefit from low-cost high-throughput sequencing, but require longer read lengths. We demonstrate that our approach enables metagenomic analyses using the Illumina Genome Analyzer, with low error rates, and at a fraction of the cost of pyrosequencing.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0011840

Cites

23 of 23 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Shera merges reads by maximizing the number of matches between the paired-end reads.
“Shera merges the reads by maximizing the number of matches between the paired-end reads.”
From PEAR: a fast and accurate Illumina Paired-End reAd mergeR (2014) · cites this paper as Rodrigue et al., 2010
Both Shera and FLASH ignore the quality scores of the base calls.
“Both, Shera and FLASH (see later in the text) ignore the quality scores of the base calls.”
From PEAR: a fast and accurate Illumina Paired-End reAd mergeR (2014) · cites this paper as Rodrigue et al., 2010
Shera merges all reads and leaves it to the user to decide which merged reads are correct.
“Shera merges all reads and leaves it to the user to decide which merged reads are correct.”
From PEAR: a fast and accurate Illumina Paired-End reAd mergeR (2014) · cites this paper as Rodrigue et al., 2010

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
Base-Calling of Automated Sequencer Traces Using Phred. I. Accuracy AssessmentPreprint
Ewing, B., Hillier, L., Wendl, M. C., & Green, P. (1998) · Genome Research · doi:10.1101/gr.8.3.175 · Cited by 6,993 · see citing works
Base-Calling of Automated Sequencer Traces Using Phred. II. Error Probabilities
Ewing, B., & Green, P. (1998) · Genome Research · doi:10.1101/gr.8.3.186 · Cited by 5,439 · see citing works
Accurate whole human genome sequencing using reversible terminator chemistry
Bentley, D. R., Balasubramanian, S., Swerdlow, H. P., Smith, G. P., Milton, J., Brown, C. G., Hall, K. P., Evers, D. J., Barnes, C. L., Bignell, H. R., et al. (2008) · Nature · doi:10.1038/nature07517 · Cited by 3,684 · see citing works
MEGAN analysis of metagenomic dataPreprint
Huson, D. H., Auch, A. F., Qi, J., & Schuster, S. C. (2007) · Genome Research · doi:10.1101/gr.5969107 · Cited by 3,293 · see citing works
Mapping short DNA sequencing reads and calling variants using mapping quality scores
Li, H., Ruan, J., & Durbin, R. (2008) · Genome Research · doi:10.1101/gr.078212.108 · Cited by 2,638 · see citing works
Next-generation sequencing transforms today's biology
Schuster, S. C. (2007) · Nature Methods · doi:10.1038/nmeth1156 · Cited by 1,813 · see citing works
An improved PCR method for walking in uncloned genomic DNA
Siebert, P. D., Chenchik, A. A., Kellogg, D. E., Lukyanov, K. A., & Lukyanov, S. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.6.1087 · Cited by 1,014 · see citing works
Patterns and Implications of Gene Gain and Loss in the Evolution of Prochlorococcus
Kettler, G. C., Martiny, A. C., Huang, K. H., Zucker, J., Coleman, M. L., Rodrigue, S., Chen, F., Lapidus, A. L., Ferriera, S., Johnson, J. H., et al. (2007) · PLoS Genetics · doi:10.1371/journal.pgen.0030231 · Cited by 552 · see citing works
Phymm and PhymmBL: metagenomic phylogenetic classification with interpolated Markov models
Brady, A., & Salzberg, S. L. (2009) · Nature Methods · doi:10.1038/nmeth.1358 · Cited by 526 · see citing works
Solid-phase reversible immobilization for the isolation of PCR products
DeAngelis, M. M., Wang, D. G., & Hawkins, T. L. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.22.4742 · Cited by 393 · see citing works
Amplification of cDNA ends based on template-switching effect and step- out PCR
Matz, M. V. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.6.1558 · Cited by 380 · see citing works
Metagenomics: Read Length Matters
Wommack, K. E., Bhavsar, J., & Ravel, J. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.02181-07 · Cited by 317 · see citing works
Whole Genome Amplification and De novo Assembly of Single Bacterial Cells
Rodrigue, S., Malmstrom, R. R., Berlin, A. M., Birren, B. W., Henn, M. R., & Chisholm, S. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006864 · Cited by 259 · see citing works
DNA purification and isolation using a solid-phase
Hawkins, T. L., O‘Connor-Morin, T., Roy, A., & Santillan, C. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.21.4543 · Cited by 227 · see citing works
Widespread known and novel phosphonate utilization pathways in marine bacteria revealed by functional screening and metagenomic analyses
Martinez, A., Tyson, G. W., & DeLong, E. F. (2009) · Environmental Microbiology · doi:10.1111/j.1462-2920.2009.02062.x · Cited by 203 · see citing works
Parallel, tag-directed assembly of locally derived short sequence reads
Hiatt, J. B., Patwardhan, R. P., Turner, E. H., Lee, C., & Shendure, J. (2010) · Nature Methods · doi:10.1038/nmeth.1416 · Cited by 149 · see citing works
A scalable, fully automated process for construction of sequence-ready barcoded libraries for 454
Lennon, N. J., Lintner, R. E., Anderson, S. T., Alvarez, P. A., Barry, A. J., Brockman, W., Daza, R. M., Erlich, R., Giannoukos, G., Green, L., et al. (2010) · Genome biology · doi:10.1186/gb-2010-11-2-r15 · Cited by 107 · see citing works
Gene prediction in metagenomic fragments: A large scale machine learning approach
Hoff, K. J., Tech, M., Lingner, T., Daniel, R., Morgenstern, B., & Meinicke, P. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-217 · Cited by 107 · see citing works
Magnetic hydrophilic methacrylate-based polymer microspheres for genomic DNA isolation
Křížová, J., Španová, A., Rittich, B., & Horák, D. (2005) · Journal of Chromatography A · doi:10.1016/j.chroma.2004.12.014 · Cited by 89 · see citing works
Regulation of average length of complex PCR product
Shagin, D. A. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.18.e23 · Cited by 73 · see citing works
The Long March: A Sample Preparation Technique that Enhances Contig Length and Coverage by High-Throughput Short-Read Sequencing
Sorber, K., Chiu, C. Y., Webster, D. R., Dimon, M. T., Ruby, J. G., Hekele, A., & DeRisi, J. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003495 · Cited by 29 · see citing works
Short clones or long clones? A simulation study on the use of paired reads in metagenomics
Mitra, S., Schubach, M., & Huson, D. H. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-s1-s12 · Cited by 22 · see citing works

Flagged first, then by citations

1 of the 24 references couldn’t be matched to a known paper.

Sorted by citations

FLASH: fast length adjustment of short reads to improve genome assemblies
Magoč, T., & Salzberg, S. L. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr507 · Cited by 15,366 · see citing works
PEAR: a fast and accurate Illumina Paired-End reAd mergeR
Zhang, J., Kobert, K., Flouri, T., & Stamatakis, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt593 · Cited by 4,497 · see citing works
PANDAseq: paired-end assembler for Illumina sequences
Masella, A. P., Bartram, A. K., Truszkowski, J. M., Brown, D. G., & Neufeld, J. D. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-31 · Cited by 2,132 · see citing works
Error filtering, pair assembly and error correction for next-generation sequencing reads
Edgar, R. C., & Flyvbjerg, H. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv401 · Cited by 1,278 · see citing works
Next-generation transcriptome assembly
Martin, J. A., & Wang, Z. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3068 · Cited by 1,254 · see citing works
Experimental and analytical tools for studying the human microbiome
Kuczynski, J., Lauber, C. L., Walters, W. A., Parfrey, L. W., Clemente, J. C., Gevers, D., & Knight, R. D. (2011) · Nature Reviews Genetics · doi:10.1038/nrg3129 · Cited by 710 · see citing works
Sequence-specific error profile of Illumina sequencers
Nakamura, K., Oshima, T., Morimoto, T., Ikeda, S., Yoshikawa, H., Shiwa, Y., Ishikawa, S., Linak, M. C., Hirai, A. M., Takahashi, H., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr344 · Cited by 593 · see citing works
Bacterial Vesicles in Marine Ecosystems
Biller, S. J., Schubotz, F., Roggensack, S. E., Thompson, A., Summons, R. E., & Chisholm, S. W. (2014) · Science · doi:10.1126/science.1243457 · Cited by 533 · see citing works
Single-Cell Genomics Reveals Hundreds of Coexisting Subpopulations in Wild Prochlorococcus
Kashtan, N., Roggensack, S. E., Rodrigue, S., Berta-Thompson, J. W., Biller, S. J., Coe, A., Ding, H., Marttinen, P., Malmstrom, R. R., Stocker, R., et al. (2014) · Science · doi:10.1126/science.1248575 · Cited by 526 · see citing works
Incorporating 16S Gene Copy Number Information Improves Estimates of Microbial Diversity and Abundance
Kembel, S. W., Wu, M., Eisen, J. A., & Green, J. L. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002743 · Cited by 522 · see citing works
Illumina-based analysis of microbial community diversity
Degnan, P. H., & Ochman, H. (2011) · The ISME Journal · doi:10.1038/ismej.2011.74 · Cited by 421 · see citing works
Members of the human gut microbiota involved in recovery from Vibrio cholerae infection
Hsiao, A., Ahmed, A. M. S., Subramanian, S., Griffin, N. W., Drewry, L. L., Petri, W. A., Haque, R., Ahmed, T., & Gordon, J. I. (2014) · Nature · doi:10.1038/nature13738 · Cited by 387 · see citing works
Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen
Poulsen, M., Schwab, C., Borg Jensen, B., Engberg, R. M., Spang, A., Canibe, N., Højberg, O., Milinovich, G., Fragner, L., Schleper, C., et al. (2013) · Nature Communications · doi:10.1038/ncomms2432 · Cited by 361 · see citing works
GapFiller: a de novo assembly approach to fill the gap within paired reads
Nadalin, F., Vezzi, F., & Policriti, A. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-s14-s8 · Cited by 353 · see citing works
Metagenomic 16S rDNA I llumina tags are a powerful alternative to amplicon sequencing to explore diversity and structure of microbial communities
Logares, R., Sunagawa, S., Salazar, G., Cornejo‐Castillo, F. M., Ferrera, I., Sarmento, H., Hingamp, P., Ogata, H., de Vargas, C., Lima‐Mendez, G., et al. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12250 · Cited by 343 · see citing works
Microbiome profiling by Illumina sequencing of combinatorial sequence-tagged PCR products
Gloor, G. B., Hummelen, R., Macklaim, J. M., Dickson, R. J., Fernandes, A. D., MacPhee, R., & Reid, G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015406 · Cited by 330 · see citing works
The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus)
Rokyta, D. R., Lemmon, A. R., Margres, M. J., & Aronow, K. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-312 · Cited by 302 · see citing works
Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages
Ottesen, E. A., Young, C. R., Gifford, S., Eppley, J. M., Marin, R., Schuster, S. C., Scholin, C. A., & DeLong, E. F. (2014) · Science · doi:10.1126/science.1252476 · Cited by 258 · see citing works
Analysis of plant microbe interactions in the era of next generation sequencing technologies
Knief, C. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00216 · Cited by 252 · see citing works
CREST – Classification Resources for Environmental Sequence Tags
Lanzén, A., Jørgensen, S. L., Huson, D. H., Gorfer, M., Grindhaug, S. H., Jonassen, I., Øvreås, L., & Urich, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049334 · Cited by 242 · see citing works
H3K9me3-heterochromatin loss at protein-coding genes enables developmental lineage specification
Nicetto, D., Donahue, G., Jain, T., Peng, T., Sidoli, S., Sheng, L., Montavon, T., Becker, J. S., Grindheim, J. M., Blahnik, K. R., et al. (2019) · Science · doi:10.1126/science.aau0583 · Cited by 241 · see citing works
Natural Bacterial Communities Serve as Quantitative Geochemical Biosensors
Smith, M. B., Rocha, A. M., Smillie, C. S., Olesen, S. W., Paradis, C. J., Wu, L., Campbell, J. H., Fortney, J. L., Mehlhorn, T. L., Lowe, K. A., et al. (2015) · mBio · doi:10.1128/mbio.00326-15 · Cited by 234 · see citing works
Practical guidelines for B-cell receptor repertoire sequencing analysis
Yaari, G., & Kleinstein, S. H. (2015) · Genome Medicine · doi:10.1186/s13073-015-0243-2 · Cited by 224 · see citing works
Complementary seminovaginal microbiome in couples
Mändar, R., Punab, M., Borovkova, N., Lapp, E., Kiiker, R., Korrovits, P., Metspalu, A., Krjutškov, K., Nõlvak, H., Preem, J., et al. (2015) · Research in Microbiology · doi:10.1016/j.resmic.2015.03.009 · Cited by 223 · see citing works
Current opportunities and challenges in microbial metagenome analysis--a bioinformatic perspective
Teeling, H., & Glöckner, F. O. (2012) · Briefings in Bioinformatics · doi:10.1093/bib/bbs039 · Cited by 221 · see citing works
The Western English Channel contains a persistent microbial seed bank
Caporaso, J. G., Paszkiewicz, K. H., Field, D., Knight, R. D., & Gilbert, J. A. (2011) · The ISME Journal · doi:10.1038/ismej.2011.162 · Cited by 221 · see citing works
Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing
Ligi, T., Oopkaup, K., Truu, M., Preem, J., Nõlvak, H., Mitsch, W. J., Mander, Ü., & Truu, J. (2013) · Ecological Engineering · doi:10.1016/j.ecoleng.2013.09.007 · Cited by 213 · see citing works
Microbiome diversity and dysbiosis in aquaculture
Villamil, S. I., Huerlimann, R., & Jerry, D. R. (2020) · Reviews in Aquaculture · doi:10.1111/raq.12513 · Cited by 204 · see citing works
Complete Genome Sequence of Escherichia coli BW25113
Grenier, F., Matteau, D., Baby, V., & Rodrigue, S. (2014) · Genome Announcements · doi:10.1128/genomea.01038-14 · Cited by 198 · see citing works
Mutational landscape of EGFR- , MYC- , and Kras- driven genetically engineered mouse models of lung adenocarcinoma
McFadden, D. G., Politi, K., Bhutkar, A., Chen, F. K., Song, X., Pirun, M., Santiago, P. M., Kim-Kiselak, C., Platt, J. T., Lee, E., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1613601113 · Cited by 194 · see citing works
Metatranscriptomic analysis of diverse microbial communities reveals core metabolic pathways and microbiome-specific functionality
Jiang, Y., Xiong, X., Danska, J. S., & Parkinson, J. (2016) · Microbiome · doi:10.1186/s40168-015-0146-x · Cited by 180 · see citing works
Towards quantitative metagenomics of wild viruses and other ultra‐low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method
Duhaime, M. B., Deng, L., Poulos, B. T., & Sullivan, M. B. (2012) · Environmental Microbiology · doi:10.1111/j.1462-2920.2012.02791.x · Cited by 168 · see citing works
Unbiased Parallel Detection of Viral Pathogens in Clinical Samples by Use of a Metagenomic Approach
Yang, J., Yang, F., Ren, L., Xiong, Z., Wú, Z., Dong, J., Sun, L., Zhang, T., Hu, Y., Du, J., et al. (2011) · Journal of Clinical Microbiology · doi:10.1128/jcm.00273-11 · Cited by 162 · see citing works
Transcriptional response of bathypelagic marine bacterioplankton to the Deepwater Horizon oil spill
Rivers, A. R., Sharma, S., Tringe, S. G., Martin, J. V., Joye, S. B., & Moran, M. A. (2013) · The ISME Journal · doi:10.1038/ismej.2013.129 · Cited by 152 · see citing works
Rapid Whole-Genome Sequencing for Surveillance ofSalmonella entericaSerovar Enteritidis
den Bakker, H. C., Allard, M. W., Bopp, D. J., Brown, E. W., Fontana, J., Iqbal, Z., Kinney, A., Limberger, R. J., Musser, K. A., Shudt, M., et al. (2014) · Emerging infectious diseases · doi:10.3201/eid2008.131399 · Cited by 149 · see citing works
Physiology and evolution of nitrate acquisition in Prochlorococcus
Berube, P. M., Biller, S. J., Kent, A. G., Berta-Thompson, J. W., Roggensack, S. E., Roache-Johnson, K. H., Ackerman, M., Moore, L. R., Meisel, J. D., Sher, D., et al. (2014) · The ISME Journal · doi:10.1038/ismej.2014.211 · Cited by 142 · see citing works
COPE: an accurate k-mer-based pair-end reads connection tool to facilitate genome assembly
Liu, B., Yuan, J., Yiu, S.-M., Li, Z., Xie, Y., Chen, Y., Shi, Y., Zhang, H., Li, Y., Lam, T.-W., et al. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts563 · Cited by 138 · see citing works
Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles
Scully, E. D., Geib, S. M., Carlson, J. E., Tien, M., McKenna, D. D., & Hoover, K. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-1096 · Cited by 134 · see citing works
De Novo Transcriptome Assembly in Chili Pepper (Capsicum frutescens) to Identify Genes Involved in the Biosynthesis of Capsaicinoids
Liu, S.-Q., Li, W., Wu, Y., Chen, C.-M., & Lei, J.-J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0048156 · Cited by 136 · see citing works
The venom-gland transcriptome of the eastern coral snake (Micrurus fulvius) reveals high venom complexity in the intragenomic evolution of venoms
Margres, M. J., Aronow, K., Loyacano, J., & Rokyta, D. R. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-531 · Cited by 128 · see citing works
Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis
Malmstrom, R. R., Rodrigue, S., Huang, K. H., Kelly, L., Kern, S. E., Thompson, A., Roggensack, S. E., Berube, P. M., Henn, M. R., & Chisholm, S. W. (2012) · The ISME Journal · doi:10.1038/ismej.2012.89 · Cited by 114 · see citing works
Genomes of diverse isolates of the marine cyanobacterium Prochlorococcus
Biller, S. J., Berube, P. M., Berta-Thompson, J. W., Kelly, L., Roggensack, S. E., Awad, L., Roache-Johnson, K. H., Ding, H., Giovannoni, S. J., Rocap, G., et al. (2014) · Scientific Data · doi:10.1038/sdata.2014.34 · Cited by 112 · see citing works
A Microfluidic DNA Library Preparation Platform for Next-Generation Sequencing
Kim, H., Jebrail, M. J., Sinha, A., Bent, Z., Solberg, O. D., Williams, K. P., Langevin, S. A., Renzi, R. F., Vreugde, J. L. V. D., Meagher, R. J., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068988 · Cited by 110 · see citing works
The genesis of an exceptionally lethal venom in the timber rattlesnake (Crotalus horridus) revealed through comparative venom-gland transcriptomics
Rokyta, D. R., Wray, K. P., & Margres, M. J. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-394 · Cited by 108 · see citing works
Phylogenetically Distinct Bacteria Involve Extensive Dechlorination of Aroclor 1260 in Sediment-Free Cultures
Wang, S., & He, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059178 · Cited by 101 · see citing works
Species Identification and Profiling of Complex Microbial Communities Using Shotgun Illumina Sequencing of 16S rRNA Amplicon Sequences
Ong, S. H., Kukkillaya, V. U., Wilm, A., Lay, C., Ho, E. X. P., Low, L., Hibberd, M. L., & Nagarajan, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060811 · Cited by 100 · see citing works
MeFiT: merging and filtering tool for illumina paired-end reads for 16S rRNA amplicon sequencing
Parikh, H. I., Kopardé, V. N., Bradley, S. P., Buck, G. A., & Sheth, N. U. (2016) · BMC Bioinformatics · doi:10.1186/s12859-016-1358-1 · Cited by 97 · see citing works
The histone variant H2A.Z is an important regulator of enhancer activity
Brunelle, M., Nordell-Markovits, A., Rodrigue, S., Lupien, M., Jacques, P., & Gévry, N. Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv825 · Cited by 87 · see citing works
Linking activity and function to ecosystem dynamics in a coastal bacterioplankton community.
Gifford, S., Sharma, S., & Moran, M. A. (2014) · PubMed · doi:10.3389/fmicb.2014.00185 · Cited by 82 · see citing works
Tomatidine Is a Lead Antibiotic Molecule That Targets Staphylococcus aureus ATP Synthase Subunit C
Boulet, M. L., Isabelle, C., Guay, I., Brouillette, É., Langlois, J.-P., Jacques, P., Rodrigue, S., Brzeziński, R., Beauregard, P. B., Bouarab, K., et al. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.02197-17 · Cited by 79 · see citing works
Next–generation sequencing and systematics: What can a billion base pairs of DNA sequence data do for you?
Harrison, N., & Kidner, C. A. (2011) · Taxon · doi:10.1002/tax.606002 · Cited by 78 · see citing works
Community-integrated omics links dominance of a microbial generalist to fine-tuned resource usage
Muller, E. E. L., Pinel, N., Laczny, C. C., Hoopmann, M. R., Narayanasamy, S., Lebrun, L., Roume, H., Lin, J., May, P., Hicks, N. D., et al. (2014) · Nature Communications · doi:10.1038/ncomms6603 · Cited by 81 · see citing works
The development of colitis in Il10−/− mice is dependent on IL-22
Gunasekera, D. C., Ma, J., Vacharathit, V., Shah, P., Ramakrishnan, A., Uprety, P., Shen, Z.-L., Sheh, A., Brayton, C., Whary, M., et al. (2020) · Mucosal Immunology · doi:10.1038/s41385-019-0252-3 · Cited by 67 · see citing works
Dechlorination of Commercial PCBs and Other Multiple Halogenated Compounds by a Sediment-Free Culture ContainingDehalococcoidesandDehalobacter
Wang, S., & He, J. (2013) · Environmental Science & Technology · doi:10.1021/es4017624 · Cited by 75 · see citing works
CASPER: context-aware scheme for paired-end reads from high-throughput amplicon sequencing
Kwon, S., Lee, B., & Yoon, S. (2014) · BMC Bioinformatics · doi:10.1186/1471-2105-15-s9-s10 · Cited by 69 · see citing works
Mosaic patterns of B‐vitamin synthesis and utilization in a natural marine microbial community
Gómez‐Consarnau, L., Sachdeva, R., Gifford, S., Cutter, L. S., Fuhrman, J. A., Sañudo‐Wilhelmy, S. A., & Moran, M. A. (2018) · Environmental Microbiology · doi:10.1111/1462-2920.14133 · Cited by 68 · see citing works
Impact of host genetics on gut microbiome: Take‐home lessons from human and mouse studies
Cahana, I., & Iraqi, F. A. (2020) · Animal Models and Experimental Medicine · doi:10.1002/ame2.12134 · Cited by 61 · see citing works
The Amazon continuum dataset: quantitative metagenomic and metatranscriptomic inventories of the Amazon River plume, June 2010
Satinsky, B. M., Zielinski, B. L., Doherty, M., Smith, C. B., Sharma, S., Paul, J. H., Crump, B. C., & Moran, M. A. (2014) · Microbiome · doi:10.1186/2049-2618-2-17 · Cited by 62 · see citing works
Development of pVCR94ΔX from Vibrio cholerae, a prototype for studying multidrug resistant IncA/C conjugative plasmids
Carraro, N., Sauvé, M., Matteau, D., Lauzon, G., Rodrigue, S., & Burrus, V. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00044 · Cited by 57 · see citing works
Short-read reading-frame predictors are not created equal: sequence error causes loss of signal
Trimble, W. L., Keegan, K. P., D’Souza, M., Wilke, A., Wilkening, J., Gilbert, J. A., & Meyer, F. (2012) · BMC Bioinformatics · doi:10.1186/1471-2105-13-183 · Cited by 53 · see citing works
World-to-Digital-Microfluidic Interface Enabling Extraction and Purification of RNA from Human Whole Blood
Jebrail, M. J., Sinha, A., Vellucci, S., Renzi, R. F., Ambriz, C., Gondhalekar, C., Schoeniger, J. S., Patel, K. D., & Branda, S. S. (2014) · Analytical Chemistry · doi:10.1021/ac404085p · Cited by 51 · see citing works
A de novo metagenomic assembly program for shotgun DNA reads
Lai, B., Ding, R., Li, Y., Duan, L., & Zhu, H. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts162 · Cited by 49 · see citing works
The transcriptional response of prokaryotes to phytoplankton‐derived dissolved organic matter in seawater
Beier, S., Rivers, A. R., Moran, M. A., & Obernosterer, I. (2014) · Environmental Microbiology · doi:10.1111/1462-2920.12434 · Cited by 48 · see citing works
High‐Throughput Sequencing: A Roadmap Toward Community Ecology
Poisot, T., Péquin, B., & Gravel, D. (2013) · Ecology and Evolution · doi:10.1002/ece3.508 · Cited by 46 · see citing works
Computational Methods for High-Throughput Comparative Analyses of Natural Microbial Communities
Preheim, S. P., Perrotta, A. R., Friedman, J., Smillie, C. S., Brito, I., Smith, M. B., & Alm, E. J. (2013) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-407863-5.00018-6 · Cited by 46 · see citing works
Cloning and Transplantation of the Mesoplasma florum Genome
Baby, V., Labroussaa, F., Brodeur, J., Matteau, D., Gourgues, G., Lartigue, C., & Rodrigue, S. (2017) · ACS Synthetic Biology · doi:10.1021/acssynbio.7b00279 · Cited by 46 · see citing works
Changes in the Structure of the Microbial Community Associated with Nannochloropsis salina following Treatments with Antibiotics and Bioactive Compounds
Geng, H., Tran-Gyamfi, M. B., Lane, T. W., Sale, K. L., & Yu, E. T. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01155 · Cited by 43 · see citing works
A Microfluidic Device for Preparing Next Generation DNA Sequencing Libraries and for Automating Other Laboratory Protocols That Require One or More Column Chromatography Steps
Tan, S. J., Phan, H. L., Gerry, B. M., Kuhn, A., Hong, L. Z., Ong, Y. M., Poon, P. S. Y., Unger, M., Jones, R. C., Quake, S. R., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064084 · Cited by 42 · see citing works
Measuring the microbiome: perspectives on advances in DNA-based techniques for exploring microbial life
Foster, J. A., Bunge, J., Gilbert, J. A., & Moore, J. H. (2012) · Briefings in Bioinformatics · doi:10.1093/bib/bbr080 · Cited by 43 · see citing works
Preparation of Metagenomic Libraries from Naturally Occurring Marine Viruses
Solonenko, S. A., & Sullivan, M. B. (2013) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-407863-5.00008-3 · Cited by 38 · see citing works
Comparative Analysis of Mobilizable Genomic Islands
Daccord, A., Ceccarelli, D., Rodrigue, S., & Burrus, V. (2012) · Journal of Bacteriology · doi:10.1128/jb.01985-12 · Cited by 39 · see citing works
Identification, Characterization, and Diel Pattern of Expression of Canonical Clock Genes in Nephrops norvegicus (Crustacea: Decapoda) Eyestalk
Sbragaglia, V., Lamanna, F., Mat, A. M., Rotllant, G., Joly, S., Ketmaier, V., de la Iglesia, H. O., & Aguzzi, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141893 · Cited by 36 · see citing works
Peregrine
Langevin, S. A., Bent, Z., Solberg, O. D., Curtis, D. J., Lane, P. D., Williams, K. P., Schoeniger, J. S., Sinha, A., Lane, T. W., & Branda, S. S. (2013) · RNA Biology · doi:10.4161/rna.24284 · Cited by 36 · see citing works
Technical Evaluation: Identification of Pathogenic Mutations in PKD1 and PKD2 in Patients with Autosomal Dominant Polycystic Kidney Disease by Next-Generation Sequencing and Use of a Comprehensive New Classification System
Kinoshita, M., Higashihara, E., Kawano, H., Higashiyama, R., Koga, D., Fukui, T., Gondo, N., Oka, T., Kawahara, K., Rigó, K., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166288 · Cited by 36 · see citing works
Metagenomics — A Technological Drift in Bioremediation
Devarapalli, P., & Kumavath, R. (2015) · InTech eBooks · doi:10.5772/60749 · Cited by 35 · see citing works
In-depth analysis of interrelation between quality scores and real errors in illumina reads
Kwon, S., Park, S., Lee, B., & Yoon, S. (2013) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/embc.2013.6609580 · Cited by 35 · see citing works
Diminishing return for increased Mappability with longer sequencing reads: implications of the k-mer distributions in the human genome
Li, W., Freudenberg, J., & Miramontes, P. (2014) · BMC Bioinformatics · doi:10.1186/1471-2105-15-2 · Cited by 34 · see citing works
Taxonomic and Functional Metagenomic Signature of Turfs in the Abrolhos Reef System (Brazil)
Walter, J. M., Tschoeke, D. A., Meirelles, P. M., de Oliveira, L., Leomil, L., Tenório, M. M. B., Valle, R., Salomon, P. S., Thompson, C. C., & Thompson, F. L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161168 · Cited by 30 · see citing works
Viruses of the Nahant Collection, characterization of 251 marine Vibrionaceae viruses
Kauffman, K. M., Brown, J. M., Sharma, R. S., VanInsberghe, D., Elsherbini, J., Polz, M. F., & Kelly, L. (2018) · Scientific Data · doi:10.1038/sdata.2018.114 · Cited by 30 · see citing works
Metatranscriptomics of N2-fixing cyanobacteria in the Amazon River plume
Hilton, J. A., Satinsky, B. M., Doherty, M., Zielinski, B. L., & Zehr, J. P. (2014) · The ISME Journal · doi:10.1038/ismej.2014.240 · Cited by 29 · see citing works
Prevention, diagnosis and treatment of high‐throughput sequencing data pathologies
Zhou, X., & Rokas, A. (2014) · Molecular Ecology · doi:10.1111/mec.12680 · Cited by 29 · see citing works
Analyzing Functional Microbial Diversity
Srivastava, N., Gupta, B., Gupta, S., Danquah, M. K., & Sarethy, I. P. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814849-5.00006-x · Cited by 28 · see citing works
Microbial diversity and activity in the Nematostella vectensis holobiont: insights from 16S rRNA gene sequencing, isolate genomes, and a pilot-scale survey of gene expression
Har, J. Y., Helbig, T., Lim, J. H., Fernando, S. C., Reitzel, A. M., Penn, K., & Thompson, J. R. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00818 · Cited by 27 · see citing works
Exploring the Plant Microbiome Through Multi-omics Approaches
López‐Mondéjar, R., Kostovčík, M., Lladó, S., Carro, L., & García‐Fraile, P. (2017) · Springer eBooks · doi:10.1007/978-981-10-4059-7_13 · Cited by 27 · see citing works
High Frequency of a Novel Filamentous Phage, VCYϕ, within an Environmental Vibrio cholerae Population
Xue, H., Xu, Y., Boucher, Y., & Polz, M. F. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.06297-11 · Cited by 27 · see citing works
A near complete snapshot of the Zea mays seedling transcriptome revealed from ultra-deep sequencing
Martin, J. A., Johnson, N. V., Gross, S., Schnable, J. C., Meng, X., Wang, M., Coleman‐Derr, D., Lindquist, E., Wei, C., Kaeppler, S. M., et al. (2014) · Scientific Reports · doi:10.1038/srep04519 · Cited by 26 · see citing works
Phenotypic plasticity in heterotrophic marine microbial communities in continuous cultures
Beier, S., Rivers, A. R., Moran, M. A., & Obernosterer, I. (2014) · The ISME Journal · doi:10.1038/ismej.2014.206 · Cited by 25 · see citing works
Draft Genome Sequence of Alteromonas macleodii Strain MIT1002, Isolated from an Enrichment Culture of the Marine Cyanobacterium Prochlorococcus
Biller, S. J., Coe, A., Martín-Cuadrado, A.-B., & Chisholm, S. W. (2015) · Genome Announcements · doi:10.1128/genomea.00967-15 · Cited by 25 · see citing works
Inferring the Minimal Genome of Mesoplasma florum by Comparative Genomics and Transposon Mutagenesis
Baby, V., Lachance, J., Gagnon, J., Lucier, J., Matteau, D., Knight, T., & Rodrigue, S. (2018) · mSystems · doi:10.1128/msystems.00198-17 · Cited by 24 · see citing works
Metagenomic Detection Methods in Biopreparedness Outbreak Scenarios
Lindsjö, O. K., Hansen, T., Knutsson, R., Löfström, C., Granberg, F., & Berg, M. (2013) · Biosecurity and Bioterrorism Biodefense Strategy Practice and Science · doi:10.1089/bsp.2012.0077 · Cited by 23 · see citing works
Multiplex sequencing of bacterial artificial chromosomes for assembling complex plant genomes
Beier, S., Himmelbach, A., Schmutzer, T., Felder, M., Taudien, S., Mayer, K., Platzer, M., Stein, N., Scholz, U., & Mascher, M. (2016) · Plant Biotechnology Journal · doi:10.1111/pbi.12511 · Cited by 23 · see citing works
Longitudinal microbiome profiling reveals impermanence of probiotic bacteria in domestic pigeons
Grond, K., Perreau, J. M., Loo, W. T., Spring, A. J., Cavanaugh, C. M., & Hird, S. M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0217804 · Cited by 23 · see citing works
Virioplankton Assemblage Structure in the Lower River and Ocean Continuum of the Amazon
Silva, B. S. D. O., Coutinho, F. H., Gregoracci, G. B., Leomil, L., de Oliveira, L. S., Fróes, A. M., Tschoeke, D. A., Soares, A. C., Cabral, A. D. S., Ward, N. D., et al. (2017) · mSphere · doi:10.1128/msphere.00366-17 · Cited by 22 · see citing works
Quantification and genome-wide mapping of DNA double-strand breaks
Grégoire, M.-C., Massonneau, J., Leduc, F., Arguin, M., Brazeau, M.-A., & Boissonneault, G. (2016) · DNA repair · doi:10.1016/j.dnarep.2016.10.005 · Cited by 22 · see citing works
Global Mapping of Open Chromatin Regulatory Elements by Formaldehyde-Assisted Isolation of Regulatory Elements Followed by Sequencing (FAIRE-seq)
Bianco, S., Rodrigue, S., Murphy, B. D., & Gévry, N. Y. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2877-4_17 · Cited by 21 · see citing works
Choice of Next-Generation Sequencing Pipelines
CHIERICO, F. D., Ancora, M., Marcacci, M., Cammà, C., Putignani, L., & Conti, S. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1720-4_3 · Cited by 21 · see citing works
Can Targeting Non-Contiguous V-Regions With Paired-End Sequencing Improve 16S rRNA-Based Taxonomic Resolution of Microbiomes?: An In Silico Evaluation
Pinna, N. K., Dutta, A., Haque, M. M., & Mande, S. S. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00653 · Cited by 20 · see citing works
The DNA double-strand “breakome” of mouse spermatids
Grégoire, M.-C., Leduc, F., Morin, M., Cavé, T., Arguin, M., Richter, M. V., Jacques, P., & Boissonneault, G. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2769-0 · Cited by 20 · see citing works
Multiple bursts of speciation in Madagascar’s endangered lemurs
Everson, K. M., Pozzi, L., Barrett, M., Blair, M. E., Donohue, M. E., Kappeler, P. M., Kitchener, A. C., Lemmon, A. R., Lemmon, E. M., Pavón‐Vázquez, C. J., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-62310-y · Cited by 20 · see citing works
Development of oriC -Based Plasmids for Mesoplasma florum
Matteau, D., Pepin, M.-E., Baby, V., Gauthier, S., Giraldo, M. A., Knight, T. F., & Rodrigue, S. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.03374-16 · Cited by 19 · see citing works

Unlocking short read sequencing for metagenomics. PLoS ONE 5(7): e11840
Materna, A. C., Timberlake, S. C., Blackburn, M. C., Malmstrom, R. R., Alm, E. J., & Chisholm, S. W. (2010)
COMPARATIVE METAGENOMIC ASSESSMENT OF SHORT- AND LONG-READ SEQUENCING TECHNOLOGIES REVEALS UNKNOWN MICROBIAL INFORMATION IN A COMPLEX ENVIRONMENTAL SAMPLEPreprint
Díaz‐Rúa, R., Drautz‐Moses, D. I., Zhao, X., Perumal, S., Esau, L. E., Angelov, A., Putra, A., Driguez, P., Cheung, M. S., & Palescandolo, E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.22.696079
Short clones or long clones? A simulation study on the use of paired reads in metagenomics
Mitra, S., Schubach, M., & Huson, D. H. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-s1-s12 · Cited by 22 · see citing works
A Filtering Method to Generate High Quality Short Reads Using Illumina Paired-End Technology
Eren, A. M., Vineis, J. H., Morrison, H. G., & Sogin, M. L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066643 · Cited by 350 · see citing works
Assessing Illumina, Nanopore and PacBio sequencing platforms at recovering high quality genomes from complex microbial communities
Sereika, M., Kirkegaard, R. H., Sørensen, E. A., Karst, S. M., Michaelsen, T. Y., & Albertsen, M. (2021) · VBN Forskningsportal (Aalborg Universitet)

Authors: Rodrigue, S., Materna, A. C., Timberlake, S. C., Blackburn, M. C., Malmstrom, R. R., Alm, E. J., & Chisholm, S. W.
Affiliations: Massachusetts Institute of Technology (US)
Corresponding author: Alm, Eric J.
Chisholm, Sallie W.
ORCID: Rodrigue, Sébastien
Blackburn, Matthew C.
Malmstrom, Rex R.
Alm, Eric J.
Chisholm, Sallie W.
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2010-07-28
Volume: 5
Issue: 7
Pages: e11840
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0011840
PMC: PMC2911387
OpenAlex: W2151671981
Cited by: 168
References: 24
Citations by year: 2025: 5 · 2024: 2 · 2023: 6 · 2022: 2 · 2021: 1 · 2020: 6 · 2019: 3 · 2018: 10 · 2017: 7 · 2016: 13 · 2015: 21 · 2014: 32 · 2013: 29 · 2012: 16
FWCI: 7.56
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
Figshare (submittedVersion, cc-by)
Funders: U.S. Department of Energy (DEFG0207ER64506)
Gordon and Betty Moore Foundation
Fonds Québécois de la Recherche sur la Nature et les Technologies
Natural Sciences and Engineering Research Council of Canada
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Physical Sciences › Environmental Science › Ecology › Environmental DNA in Biodiversity Studies
Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords: metagenomics, short-read sequencing, long-read sequencing, paired-end sequencing, sequencing cost, read length
MeSH terms: Software, Sequence Analysis, DNA, Metagenomics

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Unlocking short read sequencing for metagenomics

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks