Exception to the Rule: Genomic Characterization of Naturally Occurring Unusual Vibrio cholerae Strains with a Single Chromosome
Abstract
Here, the genetic make-up of most bacteria is encoded in a single chromosome while about 10% have more than one chromosome. Among these, Vibrio cholerae, with two chromosomes, has served as a model system to study various aspects of chromosome maintenance, mainly replication, and faithful partitioning of multipartite genomes. Here, we describe the genomic characterization of strains that are an exception to the two chromosome rules: naturally occurring single-chromosome V. cholerae. Whole genome sequence analyses of NSCV1 and NSCV2 (natural single-chromosome vibrio) revealed that the Chr1 and Chr2 fusion junctions contain prophages, IS elements, and direct repeats, in addition to large-scale chromosomal rearrangements such as inversions, insertions, and long tandem repeats elsewhere in the chromosome compared to prototypical two chromosome V. cholerae genomes. Many of the known cholera virulence factors are absent. The two origins of replication and associated genes are generally intact with synonymous mutations in some genes, as arerecAand mismatch repair (MMR) genes dam, mutH, and mutL; MutS function is probably impaired in NSCV2. These strains are ideal tools for studying mechanistic aspects of maintenance of chromosomes with multiple origins and other rearrangements and the biological, functional, and evolutionary significance of multipartite genome architecture in general.
- Authors:
-
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Morgan State Univ., Baltimore, MD (United States)
- Philipps-Univ. Marburg, Marburg (Germany)
- Tauri Group, LLC, Alexandria, VA (United States); Defense Biological Product Assurance Office, Frederick, MD (United States)
- Publication Date:
- Research Org.:
- Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
- Sponsoring Org.:
- Defense Threat Reduction Agency (DTRA); USDOE
- OSTI Identifier:
- 1398918
- Report Number(s):
- LA-UR-17-21600
Journal ID: ISSN 2314-436X
- Grant/Contract Number:
- AC52-06NA25396
- Resource Type:
- Accepted Manuscript
- Journal Name:
- International Journal of Genomics
- Additional Journal Information:
- Journal Volume: 2017; Journal ID: ISSN 2314-436X
- Publisher:
- Hindawi
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; Biological Science; V. cholerae; non-O1/non-O139 serogroup; whole genome sequencing; single chromosome; DNA adenine methyl transferase; dam; origin of replication; mismatch repair
Citation Formats
Xie, Gary, Johnson, Shannon Lyn, Davenport, Karen Walston, Rajavel, Mathumathi, Waldminghaus, Torsten, Detter, John Chris, Chain, Patrick Sam Guy, and Sozhamannan, Shanmuga. Exception to the Rule: Genomic Characterization of Naturally Occurring Unusual Vibrio cholerae Strains with a Single Chromosome. United States: N. p., 2017.
Web. doi:10.1155/2017/8724304.
Xie, Gary, Johnson, Shannon Lyn, Davenport, Karen Walston, Rajavel, Mathumathi, Waldminghaus, Torsten, Detter, John Chris, Chain, Patrick Sam Guy, & Sozhamannan, Shanmuga. Exception to the Rule: Genomic Characterization of Naturally Occurring Unusual Vibrio cholerae Strains with a Single Chromosome. United States. https://doi.org/10.1155/2017/8724304
Xie, Gary, Johnson, Shannon Lyn, Davenport, Karen Walston, Rajavel, Mathumathi, Waldminghaus, Torsten, Detter, John Chris, Chain, Patrick Sam Guy, and Sozhamannan, Shanmuga. Tue .
"Exception to the Rule: Genomic Characterization of Naturally Occurring Unusual Vibrio cholerae Strains with a Single Chromosome". United States. https://doi.org/10.1155/2017/8724304. https://www.osti.gov/servlets/purl/1398918.
@article{osti_1398918,
title = {Exception to the Rule: Genomic Characterization of Naturally Occurring Unusual Vibrio cholerae Strains with a Single Chromosome},
author = {Xie, Gary and Johnson, Shannon Lyn and Davenport, Karen Walston and Rajavel, Mathumathi and Waldminghaus, Torsten and Detter, John Chris and Chain, Patrick Sam Guy and Sozhamannan, Shanmuga},
abstractNote = {Here, the genetic make-up of most bacteria is encoded in a single chromosome while about 10% have more than one chromosome. Among these, Vibrio cholerae, with two chromosomes, has served as a model system to study various aspects of chromosome maintenance, mainly replication, and faithful partitioning of multipartite genomes. Here, we describe the genomic characterization of strains that are an exception to the two chromosome rules: naturally occurring single-chromosome V. cholerae. Whole genome sequence analyses of NSCV1 and NSCV2 (natural single-chromosome vibrio) revealed that the Chr1 and Chr2 fusion junctions contain prophages, IS elements, and direct repeats, in addition to large-scale chromosomal rearrangements such as inversions, insertions, and long tandem repeats elsewhere in the chromosome compared to prototypical two chromosome V. cholerae genomes. Many of the known cholera virulence factors are absent. The two origins of replication and associated genes are generally intact with synonymous mutations in some genes, as arerecAand mismatch repair (MMR) genes dam, mutH, and mutL; MutS function is probably impaired in NSCV2. These strains are ideal tools for studying mechanistic aspects of maintenance of chromosomes with multiple origins and other rearrangements and the biological, functional, and evolutionary significance of multipartite genome architecture in general.},
doi = {10.1155/2017/8724304},
journal = {International Journal of Genomics},
number = ,
volume = 2017,
place = {United States},
year = {2017},
month = {8}
}
Web of Science
Works referenced in this record:
Chromosome I Controls Chromosome II Replication in Vibrio cholerae
journal, February 2014
- Baek, Jong Hwan; Chattoraj, Dhruba K.
- PLoS Genetics, Vol. 10, Issue 2
Versatile and open software for comparing large genomes
journal, January 2004
- Kurtz, Stefan; Phillippy, Adam; Delcher, Arthur L.
- Genome Biology, Vol. 5, Issue 2, R12
The Pfam Protein Families Database
journal, January 2002
- Bateman, A.
- Nucleic Acids Research, Vol. 30, Issue 1
Genome Project Standards in a New Era of Sequencing
journal, October 2009
- Chain, P. S. G.; Grafham, D. V.; Fulton, R. S.
- Science, Vol. 326, Issue 5950
DNA Adenine Methylation Is Required to Replicate Both Vibrio cholerae Chromosomes Once per Cell Cycle
journal, May 2010
- Demarre, Gaëlle; Chattoraj, Dhruba K.
- PLoS Genetics, Vol. 6, Issue 5
DNAPlotter: circular and linear interactive genome visualization
journal, November 2008
- Carver, T.; Thomson, N.; Bleasby, A.
- Bioinformatics, Vol. 25, Issue 1
A probabilistic method for identifying start codons in bacterial genomes
journal, December 2001
- Suzek, B. E.; Ermolaeva, M. D.; Schreiber, M.
- Bioinformatics, Vol. 17, Issue 12
Distribution of Centromere-Like parS Sites in Bacteria: Insights from Comparative Genomics
journal, September 2007
- Livny, Jonathan; Yamaichi, Yoshiharu; Waldor, Matthew K.
- Journal of Bacteriology, Vol. 189, Issue 23
Distinct Centromere-Like parS Sites on the Two Chromosomes of Vibrio spp.
journal, May 2007
- Yamaichi, Y.; Fogel, M. A.; McLeod, S. M.
- Journal of Bacteriology, Vol. 189, Issue 14
KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000
- Kanehisa, Minoru; Goto, Susumu
- Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
par genes and the pathology of chromosome loss in Vibrio cholerae
journal, December 2006
- Yamaichi, Y.; Fogel, M. A.; Waldor, M. K.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 2
Genetic recombination and the cell cycle: what we have learned from chromosome dimers: Genetic recombination and the cell cycle
journal, October 2004
- Lesterlin, Christian; Barre, François-Xavier; Cornet, François
- Molecular Microbiology, Vol. 54, Issue 5
Vibrio cholerae O1 Isolate with Novel Genetic Background, Thailand–Myanmar
journal, June 2013
- Okada, Kazuhisa; Roobthaisong, Amonrattana; Swaddiwudhipong, Witaya
- Emerging Infectious Diseases, Vol. 19, Issue 6
The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle
journal, June 2007
- Rasmussen, Tue; Jensen, Rasmus Bugge; Skovgaard, Ole
- The EMBO Journal, Vol. 26, Issue 13
Mauve: Multiple Alignment of Conserved Genomic Sequence With Rearrangements
journal, June 2004
- Darling, A. C. E.
- Genome Research, Vol. 14, Issue 7
Distinct Replication Requirements for the Two Vibrio cholerae Chromosomes
journal, August 2003
- Egan, Elizabeth S.; Waldor, Matthew K.
- Cell, Vol. 114, Issue 4
Genome Engineering in Vibrio cholerae: A Feasible Approach to Address Biological Issues
journal, January 2012
- Val, Marie-Eve; Skovgaard, Ole; Ducos-Galand, Magaly
- PLoS Genetics, Vol. 8, Issue 1
Scanning the Landscape of Genome Architecture of Non-O1 and Non-O139 Vibrio cholerae by Whole Genome Mapping Reveals Extensive Population Genetic Diversity
journal, March 2015
- Chapman, Carol; Henry, Matthew; Bishop-Lilly, Kimberly A.
- PLOS ONE, Vol. 10, Issue 3
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997
- Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
- Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons
journal, August 2011
- Alikhan, Nabil-Fareed; Petty, Nicola K.; Ben Zakour, Nouri L.
- BMC Genomics, Vol. 12, Issue 1
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence
journal, March 1997
- Lowe, Todd M.; Eddy, Sean R.
- Nucleic Acids Research, Vol. 25, Issue 5
CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes
journal, March 2007
- Barrangou, R.; Fremaux, C.; Deveau, H.
- Science, Vol. 315, Issue 5819
Extended serotyping scheme forVibrio cholerae
journal, March 1994
- Shimada, Toshio; Arakawa, Eiji; Itoh, Kenichiro
- Current Microbiology, Vol. 28, Issue 3
DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae
journal, August 2000
- Heidelberg, John F.; Eisen, Jonathan A.; Nelson, William C.
- Nature, Vol. 406, Issue 6795
MicroReview: Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes: Multiple chromosomes in prokaryotes
journal, March 2005
- Egan, Elizabeth S.; Fogel, Michael A.; Waldor, Matthew K.
- Molecular Microbiology, Vol. 56, Issue 5
Vibrios Commonly Possess Two Chromosomes
journal, January 2005
- Okada, K.; Iida, T.; Kita-Tsukamoto, K.
- Journal of Bacteriology, Vol. 187, Issue 2
Inverted Repeat Structure of the Human Genome: The X-Chromosome Contains a Preponderance of Large, Highly Homologous Inverted Repeats That Contain Testes Genes
journal, September 2004
- Warburton, P. E.
- Genome Research, Vol. 14, Issue 10a
Replication patterns and organization of replication forks in Vibrio cholerae
journal, March 2011
- Stokke, Caroline; Waldminghaus, Torsten; Skarstad, Kirsten
- Microbiology, Vol. 157, Issue 3
Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008
- Zerbino, D. R.; Birney, E.
- Genome Research, Vol. 18, Issue 5
Enabling the democratization of the genomics revolution with a fully integrated web-based bioinformatics platform
journal, November 2016
- Li, Po-E; Lo, Chien-Chi; Anderson, Joseph J.
- Nucleic Acids Research, Vol. 45, Issue 1
The InterPro Database, 2003 brings increased coverage and new features
journal, January 2003
- Mulder, N. J.
- Nucleic Acids Research, Vol. 31, Issue 1
progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
journal, June 2010
- Darling, Aaron E.; Mau, Bob; Perna, Nicole T.
- PLoS ONE, Vol. 5, Issue 6
Gene Fitness Landscapes of Vibrio cholerae at Important Stages of Its Life Cycle
journal, December 2013
- Kamp, Heather D.; Patimalla-Dipali, Bharathi; Lazinski, David W.
- PLoS Pathogens, Vol. 9, Issue 12
The TIGRFAMs database of protein families
journal, January 2003
- Haft, D. H.
- Nucleic Acids Research, Vol. 31, Issue 1
Tandem repeats finder: a program to analyze DNA sequences
journal, January 1999
- Benson, G.
- Nucleic Acids Research, Vol. 27, Issue 2
IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis: Figure 1.
journal, April 2015
- Dhillon, Bhavjinder K.; Laird, Matthew R.; Shay, Julie A.
- Nucleic Acids Research, Vol. 43, Issue W1
Complete Genome Assemblies for Two Single-Chromosome Vibrio cholerae Isolates, Strains 1154-74 (Serogroup O49) and 10432-62 (Serogroup O27)
journal, May 2015
- Johnson, S. L.; Khiani, A.; Bishop-Lilly, K. A.
- Genome Announcements, Vol. 3, Issue 3
Development of joint application strategies for two microbial gene finders
journal, February 2004
- McHardy, A. C.; Goesmann, A.; Puhler, A.
- Bioinformatics, Vol. 20, Issue 10
Accelerated growth in the absence of DNA replication origins
journal, November 2013
- Hawkins, Michelle; Malla, Sunir; Blythe, Martin J.
- Nature, Vol. 503, Issue 7477
A checkpoint control orchestrates the replication of the two chromosomes of Vibrio cholerae
journal, April 2016
- Val, Marie-Eve; Marbouty, Martial; de Lemos Martins, Francisco
- Science Advances, Vol. 2, Issue 4
High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model–based analyses of transposon-insertion sequencing data
journal, July 2013
- Chao, Michael C.; Pritchard, Justin R.; Zhang, Yanjia J.
- Nucleic Acids Research, Vol. 41, Issue 19
Fuse or die: how to survive the loss of Dam in V ibrio cholerae : Natural fusion of
journal, January 2014
- Val, Marie-Eve; Kennedy, Sean P.; Soler-Bistué, Alfonso J.
- Molecular Microbiology, Vol. 91, Issue 4
A defined transposon mutant library and its use in identifying motility genes in Vibrio cholerae
journal, June 2008
- Cameron, D. E.; Urbach, J. M.; Mekalanos, J. J.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 25
Independent Control of Replication Initiation of the Two Vibrio cholerae Chromosomes by DnaA and RctB
journal, August 2006
- Duigou, S.; Knudsen, K. G.; Skovgaard, O.
- Journal of Bacteriology, Vol. 188, Issue 17
Determination of the transcriptome of Vibrio cholerae during intraintestinal growth and midexponential phase in vitro
journal, January 2003
- Xu, Q.; Dziejman, M.; Mekalanos, J. J.
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 3
Management of multipartite genomes: the Vibrio cholerae model
journal, December 2014
- Val, Marie-Eve; Soler-Bistué, Alfonso; Bland, Michael J.
- Current Opinion in Microbiology, Vol. 22
FtsK-Dependent Dimer Resolution on Multiple Chromosomes in the Pathogen Vibrio cholerae
journal, September 2008
- Val, Marie-Eve; Kennedy, Sean P.; El Karoui, Meriem
- PLoS Genetics, Vol. 4, Issue 9
The Two Cis-Acting Sites, parS1 and oriC1, Contribute to the Longitudinal Organisation of Vibrio cholerae Chromosome I
journal, July 2014
- David, Ariane; Demarre, Gaëlle; Muresan, Leila
- PLoS Genetics, Vol. 10, Issue 7
Comparative Genomic Characterization of a Thailand–Myanmar Isolate, MS6, of Vibrio cholerae O1 El Tor, Which Is Phylogenetically Related to a “US Gulf Coast” Clone
journal, June 2014
- Okada, Kazuhisa; Na-Ubol, Mathukorn; Natakuathung, Wirongrong
- PLoS ONE, Vol. 9, Issue 6
The Three Vibrio cholerae Chromosome II-Encoded ParE Toxins Degrade Chromosome I following Loss of Chromosome II
journal, November 2010
- Yuan, J.; Yamaichi, Y.; Waldor, M. K.
- Journal of Bacteriology, Vol. 193, Issue 3
ATP negatively regulates the initiator protein of Vibrio cholerae chromosome II replication
journal, July 2008
- Duigou, S.; Yamaichi, Y.; Waldor, M. K.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 30
Genome sequencing in microfabricated high-density picolitre reactors
journal, July 2005
- Margulies, Marcel; Egholm, Michael; Altman, William E.
- Nature, Vol. 437, Issue 7057, p. 376-380
The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003
journal, January 2003
- Boeckmann, B.
- Nucleic Acids Research, Vol. 31, Issue 1
The COG database: an updated version includes eukaryotes
journal, January 2003
- Tatusov, Roman L.; Fedorova, Natalie D.; Jackson, John D.
- BMC Bioinformatics, Vol. 4, Article No. 41
ACT: the Artemis comparison tool
journal, June 2005
- Carver, T. J.; Rutherford, K. M.; Berriman, M.
- Bioinformatics, Vol. 21, Issue 16
Chromosome dynamics in multichromosome bacteria
journal, July 2012
- Jha, Jyoti K.; Baek, Jong Hwan; Venkova-Canova, Tatiana
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1819, Issue 7
Transition from a plasmid to a chromosomal mode of replication entails additional regulators
journal, March 2011
- Venkova-Canova, T.; Chattoraj, D. K.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 15
PHAST: A Fast Phage Search Tool
journal, June 2011
- Zhou, Y.; Liang, Y.; Lynch, K. H.
- Nucleic Acids Research, Vol. 39, Issue suppl
Comprehensive Functional Analysis of the 18 Vibrio cholerae N16961 Toxin-Antitoxin Systems Substantiates Their Role in Stabilizing the Superintegron
journal, April 2015
- Iqbal, Naeem; Guérout, Anne-Marie; Krin, Evelyne
- Journal of Bacteriology, Vol. 197, Issue 13
Fast algorithms for large-scale genome alignment and comparison
journal, June 2002
- Delcher, A. L.
- Nucleic Acids Research, Vol. 30, Issue 11
Host-induced epidemic spread of the cholera bacterium
journal, June 2002
- Merrell, D. Scott; Butler, Susan M.; Qadri, Firdausi
- Nature, Vol. 417, Issue 6889
The Vibrio cholerae genome contains two unique circular chromosomes
journal, November 1998
- Trucksis, M.; Michalski, J.; Deng, Y. K.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 24
Differential Management of the Replication Terminus Regions of the Two Vibrio cholerae Chromosomes during Cell Division
journal, September 2014
- Demarre, Gaëlle; Galli, Elisa; Muresan, Leila
- PLoS Genetics, Vol. 10, Issue 9
SlmA, a Nucleoid-Associated, FtsZ Binding Protein Required for Blocking Septal Ring Assembly over Chromosomes in E. coli
journal, May 2005
- Bernhardt, Thomas G.; de Boer, Piet A. J.
- Molecular Cell, Vol. 18, Issue 5
Works referencing / citing this record:
Evolution of Genome Architecture in Archaea: Spontaneous Generation of a New Chromosome in Haloferax volcanii
journal, April 2018
- Ausiannikava, Darya; Mitchell, Laura; Marriott, Hannah
- Molecular Biology and Evolution, Vol. 35, Issue 8