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Title: The Epigenomic Landscape of Prokaryotes

Abstract

DNA methylation acts in concert with restriction enzymes to protect the integrity of prokaryotic genomes. Studies in a limited number of organisms suggest that methylation also contributes to prokaryotic genome regulation, but the prevalence and properties of such non-restriction-associated methylation systems remain poorly understood. Here, we used single molecule, real-time sequencing to map DNA modifications including m6A, m4C, and m5C across the genomes of 230 diverse bacterial and archaeal species. We observed DNA methylation in nearly all (93%) organisms examined, and identified a total of 834 distinct reproducibly methylated motifs. This data enabled annotation of the DNA binding specificities of 620 DNA Methyltransferases (MTases), doubling known specificities for previously hard to study Type I, IIG and III MTases, and revealing their extraordinary diversity. Strikingly, 48% of organisms harbor active Type II MTases with no apparent cognate restriction enzyme. These active ‘orphan’ MTases are present in diverse bacterial and archaeal phyla and show motif specificities and methylation patterns consistent with functions in gene regulation and DNA replication. Our results reveal the pervasive presence of DNA methylation throughout the prokaryotic kingdoms, as well as the diversity of sequence specificities and potential functions of DNA methylation systems.

Authors:
 [1];  [2];  [1];  [3];  [4];  [1];  [1];  [1];  [1];  [4];  [4];  [1];  [1];  [3];  [1];  [1];  [2];  [1];  [4];  [5]
+ Show Author Affiliations
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Genomics Division; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Pacific Biosciences, Menlo Park, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division
  4. New England Biolabs, Ipswich, MA (United States)
  5. Univ. of Minnesota, Minneapolis, MN (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1379228
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 12; Journal Issue: 2; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Blow, Matthew J., Clark, Tyson A., Daum, Chris G., Deutschbauer, Adam M., Fomenkov, Alexey, Fries, Roxanne, Froula, Jeff, Kang, Dongwan D., Malmstrom, Rex R., Morgan, Richard D., Posfai, Janos, Singh, Kanwar, Visel, Axel, Wetmore, Kelly, Zhao, Zhiying, Rubin, Edward M., Korlach, Jonas, Pennacchio, Len A., Roberts, Richard J., and Fang, Gang. The Epigenomic Landscape of Prokaryotes. United States: N. p., 2016. Web. doi:10.1371/journal.pgen.1005854.
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Blow, Matthew J., Clark, Tyson A., Daum, Chris G., Deutschbauer, Adam M., Fomenkov, Alexey, Fries, Roxanne, Froula, Jeff, Kang, Dongwan D., Malmstrom, Rex R., Morgan, Richard D., Posfai, Janos, Singh, Kanwar, Visel, Axel, Wetmore, Kelly, Zhao, Zhiying, Rubin, Edward M., Korlach, Jonas, Pennacchio, Len A., Roberts, Richard J., & Fang, Gang. The Epigenomic Landscape of Prokaryotes. United States. https://doi.org/10.1371/journal.pgen.1005854
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Blow, Matthew J., Clark, Tyson A., Daum, Chris G., Deutschbauer, Adam M., Fomenkov, Alexey, Fries, Roxanne, Froula, Jeff, Kang, Dongwan D., Malmstrom, Rex R., Morgan, Richard D., Posfai, Janos, Singh, Kanwar, Visel, Axel, Wetmore, Kelly, Zhao, Zhiying, Rubin, Edward M., Korlach, Jonas, Pennacchio, Len A., Roberts, Richard J., and Fang, Gang. Fri . "The Epigenomic Landscape of Prokaryotes". United States. https://doi.org/10.1371/journal.pgen.1005854. https://www.osti.gov/servlets/purl/1379228.
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@article{osti_1379228,
title = {The Epigenomic Landscape of Prokaryotes},
author = {Blow, Matthew J. and Clark, Tyson A. and Daum, Chris G. and Deutschbauer, Adam M. and Fomenkov, Alexey and Fries, Roxanne and Froula, Jeff and Kang, Dongwan D. and Malmstrom, Rex R. and Morgan, Richard D. and Posfai, Janos and Singh, Kanwar and Visel, Axel and Wetmore, Kelly and Zhao, Zhiying and Rubin, Edward M. and Korlach, Jonas and Pennacchio, Len A. and Roberts, Richard J. and Fang, Gang},
abstractNote = {DNA methylation acts in concert with restriction enzymes to protect the integrity of prokaryotic genomes. Studies in a limited number of organisms suggest that methylation also contributes to prokaryotic genome regulation, but the prevalence and properties of such non-restriction-associated methylation systems remain poorly understood. Here, we used single molecule, real-time sequencing to map DNA modifications including m6A, m4C, and m5C across the genomes of 230 diverse bacterial and archaeal species. We observed DNA methylation in nearly all (93%) organisms examined, and identified a total of 834 distinct reproducibly methylated motifs. This data enabled annotation of the DNA binding specificities of 620 DNA Methyltransferases (MTases), doubling known specificities for previously hard to study Type I, IIG and III MTases, and revealing their extraordinary diversity. Strikingly, 48% of organisms harbor active Type II MTases with no apparent cognate restriction enzyme. These active ‘orphan’ MTases are present in diverse bacterial and archaeal phyla and show motif specificities and methylation patterns consistent with functions in gene regulation and DNA replication. Our results reveal the pervasive presence of DNA methylation throughout the prokaryotic kingdoms, as well as the diversity of sequence specificities and potential functions of DNA methylation systems.},
doi = {10.1371/journal.pgen.1005854},
journal = {PLoS Genetics},
number = 2,
volume = 12,
place = {United States},
year = {Fri Feb 12 00:00:00 EST 2016},
month = {Fri Feb 12 00:00:00 EST 2016}
}
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https://doi.org/10.1371/journal.pgen.1005854
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The methylomes of six bacteria
journal, October 2012

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The complex methylome of the human gastric pathogen Helicobacter pylori
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The functions of DNA methylation by CcrM in Caulobacter crescentus: a global approach
journal, January 2014

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Type III restriction-modification enzymes: a historical perspective
journal, July 2013

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The other face of restriction: modification-dependent enzymes
journal, August 2013

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journal, September 2013

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Type II restriction endonucleases — a historical perspective and more
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ModM DNA methyltransferase methylome analysis reveals a potential role for Moraxella catarrhalis phasevarions in otitis media
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RegTransBase – a database of regulatory sequences and interactions based on literature: a resource for investigating transcriptional regulation in prokaryotes
journal, January 2013

  • Cipriano, Michael J.; Novichkov, Pavel N.; Kazakov, Alexey E.
  • BMC Genomics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2164-14-213

BREX is a novel phage resistance system widespread in microbial genomes
journal, December 2014

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    Works referencing / citing this record:

    Bacterial DNA Methylation and Methylomes
    book, January 2016

    Rational development of transformation in Clostridium thermocellum ATCC 27405 via complete methylome analysis and evasion of native restriction–modification systems
    journal, July 2019

    • Riley, Lauren A.; Ji, Lexiang; Schmitz, Robert J.
    • Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10
    • DOI: 10.1007/s10295-019-02218-x

    Metagenomic binning and association of plasmids with bacterial host genomes using DNA methylation
    journal, December 2017

    • Beaulaurier, John; Zhu, Shijia; Deikus, Gintaras
    • Nature Biotechnology, Vol. 36, Issue 1
    • DOI: 10.1038/nbt.4037

    Widespread adenine N6-methylation of active genes in fungi
    journal, May 2017

    • Mondo, Stephen J.; Dannebaum, Richard O.; Kuo, Rita C.
    • Nature Genetics, Vol. 49, Issue 6
    • DOI: 10.1038/ng.3859

    Metaepigenomic analysis reveals the unexplored diversity of DNA methylation in an environmental prokaryotic community
    journal, January 2019

    SspABCD–SspE is a phosphorothioation-sensing bacterial defence system with broad anti-phage activities
    journal, April 2020

    The complete methylome of an entomopathogenic bacterium reveals the existence of loci with unmethylated Adenines
    journal, August 2018

    Genetic variation regulates the activation and specificity of Restriction-Modification systems in Neisseria gonorrhoeae
    journal, October 2019

    Colorectal cancer-associated microbiota contributes to oncogenic epigenetic signatures
    journal, November 2019

    • Sobhani, Iradj; Bergsten, Emma; Couffin, Séverine
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 48
    • DOI: 10.1073/pnas.1912129116

    iDNA4mC: identifying DNA N4-methylcytosine sites based on nucleotide chemical properties
    journal, July 2017

    Genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Cercospora sojina Hara on soybean
    journal, September 2017

    Identification of the DNA methyltransferases establishing the methylome of the cyanobacterium Synechocystis sp. PCC 6803
    journal, February 2018

    • Hagemann, Martin; Gärtner, Katrin; Scharnagl, Matthias
    • DNA Research, Vol. 25, Issue 4
    • DOI: 10.1093/dnares/dsy006

    Insights into Epigenome Evolution from Animal and Plant Methylomes
    journal, September 2017

    MethSMRT: an integrative database for DNA N6-methyladenine and N4-methylcytosine generated by single-molecular real-time sequencing
    journal, October 2016

    • Ye, Pohao; Luan, Yizhao; Chen, Kaining
    • Nucleic Acids Research, Vol. 45, Issue D1
    • DOI: 10.1093/nar/gkw950

    Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics
    journal, February 2018

    • Ardui, Simon; Ameur, Adam; Vermeesch, Joris R.
    • Nucleic Acids Research, Vol. 46, Issue 5
    • DOI: 10.1093/nar/gky066

    Activation of the mismatch-specific endonuclease EndoMS/NucS by the replication clamp is required for high fidelity DNA replication
    journal, May 2018

    • Ishino, Sonoko; Skouloubris, Stéphane; Kudo, Hanae
    • Nucleic Acids Research, Vol. 46, Issue 12
    • DOI: 10.1093/nar/gky460

    Phasevarions of bacterial pathogens – phase-variable epigenetic regulators evolving from restriction–modification systems
    journal, September 2019

    • Phillips, Zachary N.; Husna, Asma-Ul; Jennings, Michael P.
    • Microbiology, Vol. 165, Issue 9
    • DOI: 10.1099/mic.0.000805

    DNA Methylation by Restriction Modification Systems Affects the Global Transcriptome Profile in Borrelia burgdorferi
    journal, July 2018

    • Casselli, Timothy; Tourand, Yvonne; Scheidegger, Adam
    • Journal of Bacteriology
    • DOI: 10.1101/375352

    The Patchy Distribution of Restriction-Modification System Genes and the Conservation of Orphan Methyltransferases in Halobacteria
    journal, March 2019

    • Fullmer, Matthew S.; Ouellette, Matthew; Louyakis, Artemis S.
    • Genes
    • DOI: 10.1101/551721

    Genetic variation regulates the activation and specificity of Restriction-Modification systems in Neisseria gonorrhoeae
    journal, May 2019

    • Sánchez-Busó, Leonor; Golparian, Daniel; Parkhill, Julian
    • Scientific Reports
    • DOI: 10.1101/630434

    Mapping and characterizing N6-methyladenine in eukaryotic genomes using single-molecule real-time sequencing
    journal, May 2018

    • Zhu, Shijia; Beaulaurier, John; Deikus, Gintaras
    • Genome Research, Vol. 28, Issue 7
    • DOI: 10.1101/gr.231068.117

    The impact of DNA methylation in Alphaproteobacteria
    journal, September 2018

    • Mouammine, Annabelle; Collier, Justine
    • Molecular Microbiology, Vol. 110, Issue 1
    • DOI: 10.1111/mmi.14079

    Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme ) and its bacterial endosymbionts
    journal, October 2018

    • Sun, Xuepeng; Chen, Wenbo; Ivanov, Sergey
    • New Phytologist, Vol. 221, Issue 3
    • DOI: 10.1111/nph.15472

    DNA Methylation by Restriction Modification Systems Affects the Global Transcriptome Profile in Borrelia burgdorferi
    journal, September 2018

    • Casselli, Timothy; Tourand, Yvonne; Scheidegger, Adam
    • Journal of Bacteriology, Vol. 200, Issue 24
    • DOI: 10.1128/jb.00395-18

    Genomewide Dam Methylation in Escherichia coli during Long-Term Stationary Phase
    journal, December 2016

    Statistical modelling of CG interdistance across multiple organisms
    journal, October 2018

    First genome sequencing and comparative analyses of Corynebacterium pseudotuberculosis strains from Mexico
    journal, October 2018

    • Parise, Doglas; Parise, Mariana T. D.; Viana, Marcus V. C.
    • Standards in Genomic Sciences, Vol. 13, Issue 1
    • DOI: 10.1186/s40793-018-0325-z

    DNA methylation from a Type I restriction modification system influences gene expression and virulence in Streptococcus pyogenes
    journal, June 2019

    Reviving the Transcriptome Studies: An Insight Into the Emergence of Single-Molecule Transcriptome Sequencing
    journal, April 2019

    CVm6A: A Visualization and Exploration Database for m6As in Cell Lines
    journal, February 2019

    Characterizing the DNA Methyltransferases of Haloferax volcanii via Bioinformatics, Gene Deletion, and SMRT Sequencing
    journal, February 2018

    • Ouellette, Matthew; Gogarten, J.; Lajoie, Jessica
    • Genes, Vol. 9, Issue 3
    • DOI: 10.3390/genes9030129

    Mechanisms of DNA Methyltransferase Recruitment in Mammals
    journal, December 2018

    Epigenetic Methylations on N6-Adenine and N6-Adenosine with the same Input but Different Output
    journal, June 2019

    • Li, Zhiqing; Zhao, Ping; Xia, Qingyou
    • International Journal of Molecular Sciences, Vol. 20, Issue 12
    • DOI: 10.3390/ijms20122931

    Distribution of Type I Restriction–Modification Systems in Streptococcus suis: An Outlook
    journal, November 2016

    Genome-wide systematic identification of methyltransferase recognition and modification patterns
    journal, August 2019

    • Jensen, Torbjørn Ølshøj; Tellgren-Roth, Christian; Redl, Stephanie
    • Nature Communications, Vol. 10, Issue 1
    • DOI: 10.1038/s41467-019-11179-9

    A new marseillevirus isolated in Southern Brazil from Limnoperna fortunei
    journal, October 2016

    • dos Santos, Raíssa Nunes; Campos, Fabrício Souza; Medeiros de Albuquerque, Nathalia Rammé
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep35237

    Phase-variable bacterial loci: how bacteria gamble to maximise fitness in changing environments
    journal, July 2019

    • Phillips, Zachary N.; Tram, Greg; Seib, Kate L.
    • Biochemical Society Transactions, Vol. 47, Issue 4
    • DOI: 10.1042/bst20180633

    Convergence of DNA methylation and phosphorothioation epigenetics in bacterial genomes
    journal, April 2017

    • Chen, Chao; Wang, Lianrong; Chen, Si
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 17
    • DOI: 10.1073/pnas.1702450114

    Genetic variation regulates the activation and specificity of Restriction-Modification systems in Neisseria gonorrhoeae
    text, January 2019

    • Sánchez-Busó, Leonor; Golparian, Daniel; Parkhill, Julian
    • Apollo - University of Cambridge Repository
    • DOI: 10.17863/cam.47734

    Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria
    journal, December 2017

    • Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.02340

    The Patchy Distribution of Restriction–Modification System Genes and the Conservation of Orphan Methyltransferases in Halobacteria
    journal, March 2019

    • Fullmer, Matthew S.; Ouellette, Matthew; Louyakis, Artemis S.
    • Genes, Vol. 10, Issue 3
    • DOI: 10.3390/genes10030233

    Metaepigenomic analysis reveals the unexplored diversity of DNA methylation in an environmental prokaryotic community
    journal, August 2018

    • Hiraoka, Satoshi; Okazaki, Yusuke; Anda, Mizue
    • Nature Communications
    • DOI: 10.1101/380360

    Roles of adenosine and cytosine methylation changes and genetic mutations in adaptation to different temperatures
    journal, March 2021

    • Bruneaux, Matthieu; Kronholm, Ilkka; Ashrafi, Roghaieh
    • Epigenetics
    • DOI: 10.1101/822080

    The DNA methylation landscape of giant viruses
    journal, May 2020

    Rational development of transformation in Clostridium thermocellum ATCC 27405 via complete methylome analysis and evasion of native restriction–modification systems
    journal, July 2019

    • Riley, Lauren A.; Ji, Lexiang; Schmitz, Robert J.
    • Journal of Industrial Microbiology & Biotechnology, Vol. 46, Issue 9-10
    • DOI: 10.1007/s10295-019-02218-x

    Metagenomic binning and association of plasmids with bacterial host genomes using DNA methylation
    journal, December 2017

    • Beaulaurier, John; Zhu, Shijia; Deikus, Gintaras
    • Nature Biotechnology, Vol. 36, Issue 1
    • DOI: 10.1038/nbt.4037

    A role for the bacterial GATC methylome in antibiotic stress survival
    journal, March 2016

    • Cohen, Nadia R.; Ross, Christian A.; Jain, Saloni
    • Nature Genetics, Vol. 48, Issue 5
    • DOI: 10.1038/ng.3530

    Detecting differential DNA methylation from sequencing of bisulfite converted DNA of diverse species
    journal, July 2017

    • Huh, Iksoo; Wu, Xin; Park, Taesung
    • Briefings in Bioinformatics, Vol. 20, Issue 1
    • DOI: 10.1093/bib/bbx077

    Genome sequencing and comparative genomics reveal the potential pathogenic mechanism of Cercospora sojina Hara on soybean
    journal, September 2017

    Insights into Epigenome Evolution from Animal and Plant Methylomes
    journal, September 2017

    Contribution of DNA adenine methylation to gene expression heterogeneity inSalmonella enterica
    journal, September 2020

    • Sánchez-Romero, María A.; Olivenza, David R.; Gutiérrez, Gabriel
    • Nucleic Acids Research, Vol. 48, Issue 21
    • DOI: 10.1093/nar/gkaa730

    MethSMRT: an integrative database for DNA N6-methyladenine and N4-methylcytosine generated by single-molecular real-time sequencing
    journal, October 2016

    • Ye, Pohao; Luan, Yizhao; Chen, Kaining
    • Nucleic Acids Research, Vol. 45, Issue D1
    • DOI: 10.1093/nar/gkw950

    DNA target recognition domains in the Type I restriction and modification systems of Staphylococcus aureus
    journal, February 2017

    • Cooper, Laurie P.; Roberts, Gareth A.; White, John H.
    • Nucleic Acids Research, Vol. 45, Issue 6
    • DOI: 10.1093/nar/gkx067

    Single molecule real-time (SMRT) sequencing comes of age: applications and utilities for medical diagnostics
    journal, February 2018

    • Ardui, Simon; Ameur, Adam; Vermeesch, Joris R.
    • Nucleic Acids Research, Vol. 46, Issue 5
    • DOI: 10.1093/nar/gky066

    MetClo: methylase-assisted hierarchical DNA assembly using a single type IIS restriction enzyme
    journal, July 2018

    Epigenetic inheritance systems contribute to the evolution of a germline
    journal, August 2016

    • Lachmann, Michael; Libby, Eric
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1701
    • DOI: 10.1098/rstb.2015.0445

    Metaepigenomic analysis reveals the unexplored diversity of DNA methylation in an environmental prokaryotic community
    journal, August 2018

    • Hiraoka, Satoshi; Okazaki, Yusuke; Anda, Mizue
    • Nature Communications
    • DOI: 10.1101/380360

    Genomewide Dam Methylation in Escherichia coli during Long-Term Stationary Phase
    journal, December 2016

    Statistical modelling of CG interdistance across multiple organisms
    journal, October 2018

    First genome sequencing and comparative analyses of Corynebacterium pseudotuberculosis strains from Mexico
    journal, October 2018

    • Parise, Doglas; Parise, Mariana T. D.; Viana, Marcus V. C.
    • Standards in Genomic Sciences, Vol. 13, Issue 1
    • DOI: 10.1186/s40793-018-0325-z

    Comparative Analysis of Ralstonia solanacearum Methylomes
    collection, January 2017

    Comparative Methylome Analysis of the Occasional Ruminant Respiratory Pathogen Bibersteinia trehalosi
    journal, August 2016

    Genetic variation regulates the activation and specificity of Restriction-Modification systems in Neisseria gonorrhoeae.
    journalarticle, January 2019

    • Sánchez-Busó, Leonor; Golparian, Daniel; Parkhill, Julian
    • Springer Science and Business Media LLC
    • DOI: 10.17863/cam.46134

    Reviving the Transcriptome Studies: An Insight Into the Emergence of Single-Molecule Transcriptome Sequencing
    journal, April 2019

    Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria
    journal, December 2017

    • Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric
    • Frontiers in Microbiology, Vol. 8
    • DOI: 10.3389/fmicb.2017.02340

    Transgenerational Epigenetic Inheritance Under Environmental Stress by Genome-Wide DNA Methylation Profiling in Cyanobacterium
    journal, July 2018

    N4-Cytosine DNA Methylation Is Involved in the Maintenance of Genomic Stability in Deinococcus radiodurans
    journal, August 2019

    Chromatin Evolution-Key Innovations Underpinning Morphological Complexity
    journal, April 2019

    • Hajheidari, Mohsen; Koncz, Csaba; Bucher, Marcel
    • Frontiers in Plant Science, Vol. 10
    • DOI: 10.3389/fpls.2019.00454

    The Patchy Distribution of Restriction–Modification System Genes and the Conservation of Orphan Methyltransferases in Halobacteria
    journal, March 2019

    • Fullmer, Matthew S.; Ouellette, Matthew; Louyakis, Artemis S.
    • Genes, Vol. 10, Issue 3
    • DOI: 10.3390/genes10030233

    Mechanisms of DNA Methyltransferase Recruitment in Mammals
    journal, December 2018

    Epigenetic Methylations on N6-Adenine and N6-Adenosine with the same Input but Different Output
    journal, June 2019

    • Li, Zhiqing; Zhao, Ping; Xia, Qingyou
    • International Journal of Molecular Sciences, Vol. 20, Issue 12
    • DOI: 10.3390/ijms20122931
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