Genome Replication in Thermococcus kodakarensis Independent of Cdc6 and an Origin of Replication

Gehring, Alexandra M.; Astling, David P.; Matsumi, Rie; Burkhart, Brett W.; Kelman, Zvi; Reeve, John N.; Jones, Kenneth L.; Santangelo, Thomas J.

doi:10.3389/fmicb.2017.02084

Genome Replication in Thermococcus kodakarensis Independent of Cdc6 and an Origin of Replication

Journal Article · Fri Oct 27 00:00:00 EDT 2017 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2017.02084· OSTI ID:1903805

Gehring, Alexandra M. ^[1]; Astling, David P. ^[2]; Matsumi, Rie ^[3]; Burkhart, Brett W. ^[4]; Kelman, Zvi ^[5]; Reeve, John N. ^[3]; Jones, Kenneth L. ^[2]; Santangelo, Thomas J. ^[4]

Colorado State University, Fort Collins, CO (United States); OSTI
University of Colorado School of Medicine , Aurora, CO (United States)
The Ohio State University, Columbus, OH (United States)
Colorado State University, Fort Collins, CO (United States)
National Inst. of Standards and Technology (NIST), Rockville, MD (United States); University of Maryland, Rockville, MD (United States)

The initiation of DNA replication is typically tightly regulated by proteins that form initiation complexes at specific sequences known as replication origins. In Archaea and Eukaryotes, Cdc6, a near-universally conserved protein binds and facilitates the origin-dependent assembly of the replicative apparatus. TK1901 encodes Cdc6 in Thermococcus kodakarensis but, as we report here, TK1901 and the presumed origin of replication can be deleted from the genome of this hyperthermophilic Archaeon without any detectable effects on growth, genetic competence or the ability to support autonomous plasmid replication. All regions of the genome were equally represented in the sequences generated by whole genome sequencing of DNA isolated from T. kodakarensis strains with or without TK1901, inconsistent with DNA initiation occurring at one or few origins, and instead suggestive of replication initiating at many sites distributed throughout the genome. We were unable to generate strains lacking the recombination factors, RadA or RadB, consistent with T. kodakarensis cells, that are oligoploid (7–19 genomes per cell), employing a recombination-based mechanism of DNA replication. Deletion of the previously presumed origin region reduced the long-term viability of cultures supporting the possibility that retaining an origin-based mechanism of DNA initiation provides a survival mechanism for stationary phase cells with only one genome.

View Accepted Manuscript (DOE)

Research Organization:: Colorado State University, Fort Collins, CO (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE

OSTI ID:: 1903805

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 8; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

References (68)

Escherichia coli PriA protein is essential for inducible and constitutive stable DNA replication. Masai, H.; Asai, T.; Kubota, Y. The EMBO Journal, Vol. 13, Issue 22 https://doi.org/10.1002/j.1460-2075.1994.tb06868.x	journal	November 1994
DNA Sequence and Analysis of 136 Kilobases of the Escherichia coli Genome: Organizational Symmetry around the Origin of Replication Burland, V.; Plunkett, G.; Daniels, D. L. Genomics, Vol. 16, Issue 3 https://doi.org/10.1006/geno.1993.1230	journal	June 1993
Archaeal Orc1/Cdc6 Proteins Bell, Stephen D. Subcellular Biochemistry https://doi.org/10.1007/978-94-007-4572-8_4	book	January 2012
Localized melting of duplex DNA by Cdc6/Orc1 at the DNA replication origin in the hyperthermophilic archaeon Pyrococcus furiosus Matsunaga, Fujihiko; Takemura, Kie; Akita, Masaki Extremophiles, Vol. 14, Issue 1 https://doi.org/10.1007/s00792-009-0284-9	journal	September 2009
Genetic studies on the virus-like regions in the genome of hyperthermophilic archaeon, Thermococcus kodakarensis Tagashira, Kenta; Fukuda, Wakao; Matsubara, Masaaki Extremophiles, Vol. 17, Issue 1 https://doi.org/10.1007/s00792-012-0504-6	journal	December 2012
The chromosome copy number of the hyperthermophilic archaeon Thermococcus kodakarensis KOD1 Spaans, Sebastiaan K.; van der Oost, John; Kengen, Servé W. M. Extremophiles, Vol. 19, Issue 4 https://doi.org/10.1007/s00792-015-0750-5	journal	May 2015
Molecular machines in archaeal DNA replication Beattie, Thomas R.; Bell, Stephen D. Current Opinion in Chemical Biology, Vol. 15, Issue 5 https://doi.org/10.1016/j.cbpa.2011.07.017	journal	October 2011
Specificity and Function of Archaeal DNA Replication Initiator Proteins Samson, Rachel Y.; Xu, Yanqun; Gadelha, Catarina Cell Reports, Vol. 3, Issue 2 https://doi.org/10.1016/j.celrep.2013.01.002	journal	February 2013
TFB1 or TFB2 Is Sufficient for Thermococcus kodakaraensis Viability and for Basal Transcription in Vitro Santangelo, Thomas J.; Čuboňová, L’ubomíra; James, Cindy L. Journal of Molecular Biology, Vol. 367, Issue 2 https://doi.org/10.1016/j.jmb.2006.12.069	journal	March 2007
ORC proteins: marking the start Wigley, Dale B. Current Opinion in Structural Biology, Vol. 19, Issue 1 https://doi.org/10.1016/j.sbi.2008.12.010	journal	February 2009
Mechanisms of primer RNA synthesis and D-loop/R-loop-dependent DNA replication in Escherichia coli Masai, H.; Arai, K. Biochimie, Vol. 78, Issue 11-12 https://doi.org/10.1016/s0300-9084(97)86737-5	journal	January 1996
Template switching during break-induced replication Smith, Catherine E.; Llorente, Bertrand; Symington, Lorraine S. Nature, Vol. 447, Issue 7140 https://doi.org/10.1038/nature05723	journal	April 2007
Accelerated gene evolution through replication–transcription conflicts Paul, Sandip; Million-Weaver, Samuel; Chattopadhyay, Sujay Nature, Vol. 495, Issue 7442 https://doi.org/10.1038/nature11989	journal	March 2013
Accelerated growth in the absence of DNA replication origins Hawkins, Michelle; Malla, Sunir; Blythe, Martin J. Nature, Vol. 503, Issue 7477 https://doi.org/10.1038/nature12650	journal	November 2013
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Targeted introduction of heritable point mutations into the plant mitochondrial genome Forner, Joachim; Kleinschmidt, Dennis; Meyer, Etienne H. Nature Plants, Vol. 8, Issue 3 https://doi.org/10.1038/s41477-022-01108-y	journal	March 2022
In vivo interactions of archaeal Cdc6/Orc1 and minichromosome maintenance proteins with the replication origin Matsunaga, F.; Forterre, P.; Ishino, Y. Proceedings of the National Academy of Sciences, Vol. 98, Issue 20, p. 11152-11157 https://doi.org/10.1073/pnas.191387498	journal	September 2001
RNase H confers specificity in the dnaA-dependent initiation of replication at the unique origin of the Escherichia coli chromosome in vivo and in vitro. Ogawa, T.; Pickett, G. G.; Kogoma, T. Proceedings of the National Academy of Sciences, Vol. 81, Issue 4 https://doi.org/10.1073/pnas.81.4.1040	journal	February 1984
Thermococcus kodakarensis encodes three MCM homologs but only one is essential Pan, Miao; Santangelo, Thomas J.; Li, Zhuo Nucleic Acids Research, Vol. 39, Issue 22 https://doi.org/10.1093/nar/gkr624	journal	August 2011
Multiple replication origins with diverse control mechanisms in Haloarcula hispanica Wu, Zhenfang; Liu, Jingfang; Yang, Haibo Nucleic Acids Research, Vol. 42, Issue 4 https://doi.org/10.1093/nar/gkt1214	journal	November 2013
Archaeology of Eukaryotic DNA Replication Makarova, K. S.; Koonin, E. V. Cold Spring Harbor Perspectives in Biology, Vol. 5, Issue 11 https://doi.org/10.1101/cshperspect.a012963	journal	July 2013
Complete genome sequence of the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1 and comparison with Pyrococcus genomes Fukui, T. Genome Research, Vol. 15, Issue 3 https://doi.org/10.1101/gr.3003105	journal	February 2005
Shuttle Vector Expression in Thermococcus kodakaraensis: Contributions of cis Elements to Protein Synthesis in a Hyperthermophilic Archaeon Santangelo, T. J.; Cubonova, L.; Reeve, J. N. Applied and Environmental Microbiology, Vol. 74, Issue 10 https://doi.org/10.1128/aem.00305-08	journal	March 2008
Recombinogenic Properties of Pyrococcus furiosus Strain COM1 Enable Rapid Selection of Targeted Mutants Farkas, Joel; Stirrett, Karen; Lipscomb, Gina L. Applied and Environmental Microbiology, Vol. 78, Issue 13, p. 4669-4676 https://doi.org/10.1128/aem.00936-12	journal	April 2012
Defining Components of the Chromosomal Origin of Replication of the Hyperthermophilic Archaeon Pyrococcus furiosus Needed for Construction of a Stable Replicating Shuttle Vector Farkas, Joel; Chung, Daehwan; DeBarry, Megan Applied and Environmental Microbiology, Vol. 77, Issue 18 https://doi.org/10.1128/aem.05057-11	journal	July 2011
Genome Copy Numbers and Gene Conversion in Methanogenic Archaea Hildenbrand, Catherina; Stock, Tilmann; Lange, Christian Journal of Bacteriology, Vol. 193, Issue 3 https://doi.org/10.1128/jb.01016-10	journal	February 2011
Characterization of the Replication Initiator Orc1/Cdc6 from the Archaeon Picrophilus torridus Arora, J.; Goswami, K.; Saha, S. Journal of Bacteriology, Vol. 196, Issue 2 https://doi.org/10.1128/jb.01020-13	journal	November 2013
Key Role for Sulfur in Peptide Metabolism and in Regulation of Three Hydrogenases in the Hyperthermophilic Archaeon Pyrococcus furiosus Adams, M. W. W.; Holden, J. F.; Menon, A. L. Journal of Bacteriology, Vol. 183, Issue 2 https://doi.org/10.1128/jb.183.2.716-724.2001	journal	January 2001
Affinity Purification of an Archaeal DNA Replication Protein Network Li, Zhuo; Santangelo, Thomas J.; Čuboňová, Ľubomíra mBio, Vol. 1, Issue 5 https://doi.org/10.1128/mbio.00221-10	journal	October 2010
Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription Kogoma, T. Microbiology and Molecular Biology Reviews, Vol. 61, Issue 2 https://doi.org/10.1128/mmbr.61.2.212-238.1997	journal	June 1997
Replication-biased genome organisation in the crenarchaeon Sulfolobus Andersson, Anders F.; Pelve, Erik A.; Lindeberg, Stefan BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-454	journal	January 2010
Primary transcriptome map of the hyperthermophilic archaeon Thermococcus kodakarensis Jäger, Dominik; Förstner, Konrad U.; Sharma, Cynthia M. BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-684	journal	January 2014
Genome-wide identification and characterization of replication origins by deep sequencing Xu, Jia; Yanagisawa, Yoshimi; Tsankov, Alexander M. Genome Biology, Vol. 13, Issue 4 https://doi.org/10.1186/gb-2012-13-4-r27	journal	January 2012
Genetic and Physical Mapping of DNA Replication Origins in Haloferax volcanii Norais, Cédric; Hawkins, Michelle; Hartman, Amber L. PLoS Genetics, Vol. 3, Issue 5 https://doi.org/10.1371/journal.pgen.0030077	journal	May 2007
Regulated Polyploidy in Halophilic Archaea Breuert, Sebastian; Allers, Thorsten; Spohn, Gabi PLoS ONE, Vol. 1, Issue 1 https://doi.org/10.1371/journal.pone.0000092	journal	December 2006
Diversity of DNA Replication in the Archaea Ausiannikava, Darya; Allers, Thorsten Genes, Vol. 8, Issue 2 https://doi.org/10.3390/genes8020056	journal	January 2017
An Improved Filtering Algorithm for Big Read Datasets Wedemeyer, Axel; Kliemann, Lasse; Srivastav, Anand arXiv https://doi.org/10.48550/arxiv.1610.03443	preprint	January 2016
Mapping of origin of replication in Themococcales Ojha, Krishna K.; Swati, D. Bioinformation, Vol. 5, Issue 5 https://doi.org/10.6026/97320630005213	journal	November 2010
From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline Auwera, Geraldine A.; Carneiro, Mauricio O.; Hartl, Christopher Current Protocols in Bioinformatics, Vol. 43, Issue 1 https://doi.org/10.1002/0471250953.bi1110s43	journal	October 2013
Thermococcus kodakarensis has two functional PCNA homologs but only one is required for viability Pan, Miao; Santangelo, Thomas J.; Čuboňová, Ľubomíra Extremophiles, Vol. 17, Issue 3 https://doi.org/10.1007/s00792-013-0526-8	journal	March 2013
Mechanisms of primer RNA synthesis and D-loop/R-loop-dependent DNA replication in Escherichia coli Masai, H.; Arai, K. Biochimie, Vol. 78, Issue 11-12 https://doi.org/10.1016/S0300-9084(97)86737-5	journal	January 1996
Comparative genomics reveals conserved positioning of essential genomic clusters in highly rearranged Thermococcales chromosomes Cossu, Matteo; Da Cunha, Violette; Toffano-Nioche, Claire Biochimie, Vol. 118 https://doi.org/10.1016/j.biochi.2015.07.008	journal	November 2015
DnaA and ORC: more than DNA replication initiators Scholefield, Graham; Veening, Jan-Willem; Murray, Heath Trends in Cell Biology, Vol. 21, Issue 3 https://doi.org/10.1016/j.tcb.2010.10.006	journal	March 2011
Defining the RNaseH2 enzyme-initiated ribonucleotide excision repair pathway in Archaea Heider, Margaret R.; Burkhart, Brett W.; Santangelo, Thomas J. Journal of Biological Chemistry, Vol. 292, Issue 21 https://doi.org/10.1074/jbc.M117.783472	journal	May 2017
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Genomewide and biochemical analyses of DNA-binding activity of Cdc6/Orc1 and Mcm proteins in Pyrococcus sp. Matsunaga, Fujihiko; Glatigny, Annie; Mucchielli-Giorgi, Marie-Hélène Nucleic Acids Research, Vol. 35, Issue 10 https://doi.org/10.1093/nar/gkm212	journal	April 2007
Molecular determinants of origin discrimination by Orc1 initiators in archaea Dueber, Erin C.; Costa, Alessandro; Corn, Jacob E. Nucleic Acids Research, Vol. 39, Issue 9 https://doi.org/10.1093/nar/gkq1308	journal	January 2011
A novel mechanism for regulating the activity of proliferating cell nuclear antigen by a small protein Li, Zhuo; Huang, Richard Y. -C.; Yopp, Daniel C. Nucleic Acids Research, Vol. 42, Issue 9 https://doi.org/10.1093/nar/gku239	journal	April 2014
On the Regulation of DNA Replication in Bacteria Jacob, F.; Brenner, S.; Cuzin, F. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 28, Issue 0 https://doi.org/10.1101/SQB.1963.028.01.048	journal	January 1963
Comparative analyses of the two proliferating cell nuclear antigens from the hyperthermophilic archaeon, Thermococcus kodakarensis Kuba, Yumani; Ishino, Sonoko; Yamagami, Takeshi Genes to Cells, Vol. 17, Issue 11 https://doi.org/10.1111/gtc.12007	journal	October 2012
Origins of DNA replication in the three domains of life Robinson, Nicholas P.; Bell, Stephen D. FEBS Journal, Vol. 272, Issue 15 https://doi.org/10.1111/j.1742-4658.2005.04768.x	journal	July 2005
Mapping of active replication originsin vivoin thaum- and euryarchaeal replicons Pelve, Erik A.; Martens-Habbena, Willm; Stahl, David A. Molecular Microbiology, Vol. 90, Issue 3 https://doi.org/10.1111/mmi.12382	journal	September 2013
Replication of theEscherichia colichromosome in RNase HI-deficient cells: multiple initiation regions and fork dynamics Maduike, Nkabuije Z.; Tehranchi, Ashley K.; Wang, Jue D. Molecular Microbiology, Vol. 91, Issue 1 https://doi.org/10.1111/mmi.12440	journal	November 2013
Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Kogoma, T. Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 2 https://doi.org/10.1128/.61.2.212-238.1997	journal	January 1997
Shuttle Vector Expression in Thermococcus kodakaraensis: Contributions of cis Elements to Protein Synthesis in a Hyperthermophilic Archaeon Santangelo, T. J.; Cubonova, L.; Reeve, J. N. Applied and Environmental Microbiology, Vol. 74, Issue 10 https://doi.org/10.1128/AEM.00305-08	journal	March 2008
Recombinogenic Properties of Pyrococcus furiosus Strain COM1 Enable Rapid Selection of Targeted Mutants Farkas, Joel; Stirrett, Karen; Lipscomb, Gina L. Applied and Environmental Microbiology, Vol. 78, Issue 13, p. 4669-4676 https://doi.org/10.1128/AEM.00936-12	journal	April 2012
Defining Components of the Chromosomal Origin of Replication of the Hyperthermophilic Archaeon Pyrococcus furiosus Needed for Construction of a Stable Replicating Shuttle Vector Farkas, Joel; Chung, Daehwan; DeBarry, Megan Applied and Environmental Microbiology, Vol. 77, Issue 18 https://doi.org/10.1128/AEM.05057-11	journal	July 2011
Purification and characterization of a thermostable thiol protease from a newly isolated hyperthermophilic Pyrococcus sp. Morikawa, M.; Izawa, Y.; Rashid, N. Applied and Environmental Microbiology, Vol. 60, Issue 12 https://doi.org/10.1128/AEM.60.12.4559-4566.1994	journal	January 1994
Genome Copy Numbers and Gene Conversion in Methanogenic Archaea Hildenbrand, Catherina; Stock, Tilmann; Lange, Christian Journal of Bacteriology, Vol. 193, Issue 3 https://doi.org/10.1128/JB.01016-10	journal	February 2011
Archaeal DNA Polymerase D but Not DNA Polymerase B Is Required for Genome Replication in Thermococcus kodakarensis Cubonova, L.; Richardson, T.; Burkhart, B. W. Journal of Bacteriology, Vol. 195, Issue 10 https://doi.org/10.1128/JB.02037-12	journal	March 2013
Key Role for Sulfur in Peptide Metabolism and in Regulation of Three Hydrogenases in the Hyperthermophilic Archaeon Pyrococcus furiosus Adams, M. W. W.; Holden, J. F.; Menon, A. L. Journal of Bacteriology, Vol. 183, Issue 2 https://doi.org/10.1128/JB.183.2.716-724.2001	journal	January 2001
DNA Replication in the Archaea Barry, E. R.; Bell, S. D. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 4 https://doi.org/10.1128/MMBR.00029-06	journal	December 2006
Affinity Purification of an Archaeal DNA Replication Protein Network Li, Zhuo; Santangelo, Thomas J.; Čuboňová, Ľubomíra mBio, Vol. 1, Issue 5 https://doi.org/10.1128/mBio.00221-10	journal	October 2010
DnaA, ORC, and Cdc6: similarity beyond the domains of life and diversityThis paper is one of a selection of papers published in this special issue entitled 8th International Conference on AAA Proteins and has undergone the Journal's usual peer review process. Kawakami, Hironori; Katayama, Tsutomu Biochemistry and Cell Biology, Vol. 88, Issue 1 https://doi.org/10.1139/o09-154	journal	February 2010
Versatile and open software for comparing large genomes Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L. Genome Biology, Vol. 5, Issue 2, R12 https://doi.org/10.1186/gb-2004-5-2-r12	journal	January 2004
Cutadapt removes adapter sequences from high-throughput sequencing reads Martin, Marcel EMBnet.journal, Vol. 17, Issue 1 https://doi.org/10.14806/ej.17.1.200	journal	May 2011
Genetics Techniques for Thermococcus kodakarensis Hileman, Travis H.; Santangelo, Thomas J. Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00195	journal	January 2012
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w Cingolani, Pablo; Platts, Adrian; Wang, Le Lily Fly, Vol. 6, Issue 2 https://doi.org/10.4161/fly.19695	journal	April 2012

Similar Records

The Hyperthermophilic Restriction-Modification Systems of Thermococcus kodakarensis Protect Genome Integrity

Journal Article · Wed May 19 20:00:00 EDT 2021 · Frontiers in Microbiology · OSTI ID:1851954

Cdc6 ATPase activity disengages Cdc6 from the pre-replicative complex to promote DNA replication

Journal Article · Mon Aug 24 20:00:00 EDT 2015 · eLife · OSTI ID:1628831

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
DNA origins
DNA replication
Thermococcus kodakarensis
archaea
recombination

Genome Replication in Thermococcus kodakarensis Independent of Cdc6 and an Origin of Replication

Citation Formats

References (68)

Similar Records

Related Subjects