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Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing
Open accessAbstract
Single-molecule real-time (SMRT) DNA sequencing allows the systematic detection of chemical modifications such as methylation but has not previously been applied on a genome-wide scale. We used this approach to detect 49,311 putative 6-methyladenine (m6A) residues and 1,407 putative 5-methylcytosine (m5C) residues in the genome of a pathogenic Escherichia coli strain. We obtained strand-specific information for methylation sites and a quantitative assessment of the frequency of methylation at each modified position. We deduced the sequence motifs recognized by the methyltransferase enzymes present in this strain without prior knowledge of their specificity. Furthermore, we found that deletion of a phage-encoded methyltransferase-endonuclease (restriction-modification; RM) system induced global transcriptional changes and led to gene amplification, suggesting that the role of RM systems extends beyond protecting host genomes from foreign DNA.
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“Advanced next generation sequencing platforms such as Single Molecule Real-Time (SMRT) sequencing can be employed to reliably detect certain methylation signatures (Flusberg et al., 2010; Fang et al., 2012) as it has been done for C. autoethanogenum (Utturkar et al., 2015).”
From Gas Fermentation—A Flexible Platform for Commercial Scale Production of Low-Carbon-Fuels and Chemicals from Waste and Renewable Feedstocks (2016) · cites this paper as Fang et al., 2012
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Cites
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
Datsenko, K., & Wanner, B. (2000) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.120163297 · Cited by 15,902
MEME SUITE: tools for motif discovery and searching
Bailey, T. L., Boden, M., Buske, F. A., Frith, M., Grant, C. E., Clementi, L., Ren, J., Li, W. W., & Noble, W. S. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp335 · Cited by 10,648
A scaling normalization method for differential expression analysis of RNA-seq data
Robinson, M. D., & Oshlack, A. (2010) · Genome Biology · doi:10.1186/gb-2010-11-3-r25 · Cited by 7,876
Conversion of 5-Methylcytosine to 5-Hydroxymethylcytosine in Mammalian DNA by MLL Partner TET1
Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., et al. (2009) · Science · doi:10.1126/science.1170116 · Cited by 5,836
Kaper, J. B., Nataro, J. P., & Mobley, H. L. T. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro818 · Cited by 5,583
Guzman, L., Belin, D., Carson, M. J., & Beckwith, J. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.14.4121-4130.1995 · Cited by 4,942
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
The Nuclear DNA Base 5-Hydroxymethylcytosine Is Present in Purkinje Neurons and the Brain
Kriaucionis, S., & Heintz, N. (2009) · Science · doi:10.1126/science.1169786 · Cited by 2,700
Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility
Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005) · Science · doi:10.1126/science.1108190 · Cited by 2,563
Environmental epigenomics and disease susceptibility
Jirtle, R. L., & Skinner, M. K. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2045 · Cited by 2,492
Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning
Cokus, S. J., Feng, S.-H., Zhang, X.-Y., Chen, Z., Merriman, B., Haudenschild, C., Pradhan, S., Nelson, S., Pellegrini, M., & Jacobsen, S. (2008) · Nature · doi:10.1038/nature06745 · Cited by 2,278
Real-time DNA sequencing from single polymerase molecules.
Korlach, J., Bjornson, K., Chaudhuri, B., Cicero, R., Flusberg, B., Gray, J., Holden, D., Saxena, R., Wegener, J., & Turner, S. (2010) · Methods in Enzymology · doi:10.1016/s0076-6879(10)72001-2 · Cited by 1,847
Direct detection of DNA methylation during single-molecule, real-time sequencing
Flusberg, B. A., Webster, D. R., Lee, J. H., Travers, K. J., Olivares, E. C., Clark, T. A., Korlach, J., & Turner, S. W. (2010) · Nature Methods · doi:10.1038/nmeth.1459 · Cited by 1,460
Base-Resolution Analysis of 5-Hydroxymethylcytosine in the Mammalian Genome
Yu, M., Hon, G. C., Szulwach, K. E., Song, C., Zhang, L., Kim, A., Li, X., Dai, Q., Shen, Y., Park, B., et al. (2012) · Cell · doi:10.1016/j.cell.2012.04.027 · Cited by 1,050
A window into third-generation sequencing
Schadt, E. E., Turner, S., & Kasarskis, A. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq416 · Cited by 1,026
REBASE—a database for DNA restriction and modification: enzymes, genes and genomes
Roberts, R. J., Vincze, T., Pósfai, J., & Macelis, D. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp874 · Cited by 992
Quantitative Sequencing of 5-Methylcytosine and 5-Hydroxymethylcytosine at Single-Base Resolution
Booth, M. J., Branco, M. R., Ficz, G., Oxley, D., Krueger, F., Reik, W., & Balasubramanian, S. (2012) · Science · doi:10.1126/science.1220671 · Cited by 951
Molecular Biology of Bacteriophage T4
Karam, J. D., & Drake, J. W. (1994) · ASM Press eBooks · doi:10.1128/ecosalplus.bacteriophage-t4 · Cited by 879
Origins of the E. coli Strain Causing an Outbreak of Hemolytic–Uremic Syndrome in Germany
Rasko, D. A., Webster, D. R., Sahl, J. W., Bashir, A., Boisen, N., Scheutz, F., Paxinos, E. E., Sebra, R., Chin, C.-S., Iliopoulos, D., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1106920 · Cited by 835
The Origin of the Haitian Cholera Outbreak Strain
Chin, C.-S., Sorenson, J. M., Harris, J. B., Robins, W. P., Charles, R. C., Jean‐Charles, R. R., Bullard, J., Webster, D. R., Kasarskis, A., Peluso, P. S., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa1012928 · Cited by 747
Flagellin A is essential for the virulence of Vibrio anguillarum
Milton, D. L., O’Toole, R., Hörstedt, P., & Wolf‐Watz, H. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.5.1310-1319.1996 · Cited by 680
Epigenetic Gene Regulation in the Bacterial World
Casadesús, J., & Low, D. A. (2006) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00016-06 · Cited by 653
Parental origin of sequence variants associated with complex diseases
DIAGRAM Consortium, Kong, A., Steinthorsdottir, V., Masson, G., Thorleifsson, G., Sulem, P., Besenbacher, S., Jonasdottir, A., Sigurdsson, A., Kristinsson, K. T., et al. (2009) · Nature · doi:10.1038/nature08625 · Cited by 553
N6-methyl-adenine: an epigenetic signal for DNA–protein interactions
Wion, D., & Casadesús, J. (2006) · Nature Reviews Microbiology · doi:10.1038/nrmicro1350 · Cited by 527
An Essential Role for DNA Adenine Methylation in Bacterial Virulence
Heithoff, D. M., Sinsheimer, R. L., Low, D. A., & Mahan, M. J. (1999) · Science · doi:10.1126/science.284.5416.967 · Cited by 458
The DNA (cytosine-5) methyltransferases
Kumar, S., Cheng, X., Klimašauskas, S., Mi, S., Pósfai, J., Roberts, R. J., & Wilson, G. G. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.1.1 · Cited by 429
A flexible and efficient template format for circular consensus sequencing and SNP detection
Travers, K. J., Chin, C.-S., Rank, D. R., Eid, J. S., & Turner, S. W. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq543 · Cited by 417
Kaiser, A. D., & Jacob, F. (1957) · Virology · doi:10.1016/0042-6822(57)90083-1 · Cited by 373
IS10 transposition is regulated by DNA adenine methylation
Roberts, D. E. (1985) · Cell · doi:10.1016/0092-8674(85)90017-0 · Cited by 341
Roles of DNA Adenine Methylation in Regulating Bacterial Gene Expression and Virulence
Low, D. A., Weyand, N. J., & Mahan, M. J. (2001) · Infection and Immunity · doi:10.1128/iai.69.12.7197-7204.2001 · Cited by 337
Clark, T. A., Murray, I. A., Morgan, R., Kislyuk, A. O., Spittle, K. E., Boitano, M., Fomenkov, A. I., Roberts, R. J., & Korlach, J. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1146 · Cited by 316
Marinus, M., & Casadesús, J. (2009) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2008.00159.x · Cited by 305
A New Pyrimidine Base from Bacteriophage Nucleic Acids
Wyatt, G. R., & Cohen, S. (1952) · Nature · doi:10.1038/1701072a0 · Cited by 264
Dam methylation: coordinating cellular processes
Løbner‐Olesen, A., Skovgaard, O., & Marinus, M. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.02.009 · Cited by 252
Modified Bases in Bacteriophage DNAs
Warren, R. A. J. (1980) · Annual Review of Microbiology · doi:10.1146/annurev.mi.34.100180.001033 · Cited by 227
A cell cycle-regulated bacterial DNA methyltransferase is essential for viability.
Stephens, C. M., Reisenauer, A., Wright, R., & Shapiro, L. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.3.1210 · Cited by 206
Phasevarions Mediate Random Switching of Gene Expression in Pathogenic Neisseria
Srikhanta, Y. N., Dowideit, S. J., Edwards, J. L., Falsetta, M. L., Wu, H., Harrison, O. B., Fox, K. L., Seib, K. L., Maguire, T. L., Wang, A. H. ‐., et al. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000400 · Cited by 183
Timing and targeting: The biological functions of Dam methylation in E. coli
Messer, W., & Noyer-Weidner, M. (1988) · Cell · doi:10.1016/s0092-8674(88)90911-7 · Cited by 178
Bacterial DNA Methylation: a Cell Cycle Regulator?
Reisenauer, A., Kahng, L. S., McCollum, S., & Shapiro, L. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.17.5135-5139.1999 · Cited by 174
Epigenetic phase variation of the pap operon in Escherichia coli
van der Woude, M. W., Braaten, B. A., & Low, D. A. (1996) · Trends in Microbiology · doi:10.1016/0966-842x(96)81498-3 · Cited by 166
A DNA methylation ratchet governs progression through a bacterial cell cycle
Collier, J., McAdams, H. H., & Shapiro, L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708112104 · Cited by 166
Kahramanoglou, C., Prieto, A. I., Khedkar, S., Haase, B., Gupta, A., Beneš, V., Fraser, G. M., Luscombe, N. M., & Seshasayee, A. S. N. (2012) · Nature Communications · doi:10.1038/ncomms1878 · Cited by 156
Schadt, E. E., Banerjee, O., Fang, G., Feng, Z., Wong, W. H., Zhang, X., Kislyuk, A. O., Clark, T. A., Luong, K., Keren‐Paz, A., et al. (2012) · Genome Research · doi:10.1101/gr.136739.111 · Cited by 105
Furuta, Y., Abe, K., & Kobayashi, I. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp1226 · Cited by 85
Camacho, E. M., & Casadesús, J. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04788.x · Cited by 74
Swinton, D. C., Hattman, S., Crain, P. F., Cheng, C. S., Smith, D. L., & McCloskey, J. A. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.24.7400 · Cited by 73
Novel non-specific DNA adenine methyltransferases
Drozdz, M., Piekarowicz, A., Bujnicki, J. M., & Radlińska, M. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1039 · Cited by 61
YhdJ, a Nonessential CcrM-Like DNA Methyltransferase of Escherichia coli and Salmonella enterica
Broadbent, S. E., Balbontín, R., Casadesús, J., Marinus, M., & van der Woude, M. W. (2007) · Journal of Bacteriology · doi:10.1128/jb.01854-06 · Cited by 39
Roberts, R., & Halford, S. E. (1993) · Bristol Research (University of Bristol) · Cited by 29
Temperate Coliphage HK022: Clear Plaque Mutants and Preliminary Vegetative Map
Dhillon, T. S., & Dhillon, E. K. S. (1976) · Japanese Journal of Microbiology · doi:10.1111/j.1348-0421.1976.tb01004.x · Cited by 24
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Metadata
- Authors
- Fang, G., Munera, D., Friedman, D. I., Mandlik, A., Chao, M. C., Banerjee, O., Feng, Z., Losic, B., Mahajan, M. C., Jabado, O. J., Deikus, G., Clark, T. A., Luong, K., Murray, I. A., Davis, B. M., Keren-Paz, A., Chess, A., Roberts, R. J., Korlach, J., Turner, S. W., Kumar, V., Waldor, M. K., & Schadt, E. E.
- Affiliations
- University of Minnesota (US)
- Brigham and Women's Hospital (US)
- University of Michigan (US)
- Pacific Biosciences (United States) (US)
- Stanford University (US)
- Icahn School of Medicine at Mount Sinai (US)
- New England Biolabs (United States) (US)
- Corresponding author
- Waldor, Matthew K
- Schadt, Eric E
- ORCID
- Venue
- Nature Biotechnology
- Published
- 2012-11-08
- Volume
- 30
- Issue
- 12
- Pages
- 1232-1239
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- PMC
- PMC3879109
- OpenAlex
- W2025361601
- Cited by
- 360
- References
- 51
- Citations by year
- 2026: 7 · 2025: 21 · 2024: 19 · 2023: 19 · 2022: 24 · 2021: 24 · 2020: 29 · 2019: 30 · 2018: 36 · 2017: 19 · 2016: 25 · 2015: 44 · 2014: 31 · 2013: 25 · 2012: 4
- FWCI
- 13.38
- Type
- journal article
- Language
- en
- Update notices
- erratum (2013-06-10)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Biotechnology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation (0916439)
- Howard Hughes Medical Institute
- National Institutes of Health
- National Institute of General Medical Sciences (R44GM100560, R44GM105125)
- National Institute of Allergy and Infectious Diseases (R37AI-42347, R37AI042347)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- DNA methylation, 6-methyladenine, 5-methylcytosine, Escherichia coli, single-molecule real-time sequencing, restriction-modification systems, gene amplification, gene expression changes, genome-wide methylation mapping
- MeSH terms
- Adenine, Biotechnology, Chromosome Mapping, DNA, Bacterial, Escherichia coli, Gene Amplification, Spiro Compounds, Substrate Specificity, DNA Restriction-Modification Enzymes, Genome, Bacterial, Gene Deletion, Sequence Analysis, DNA, DNA Methylation, 5-Methylcytosine
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