Recombinant transfer in the basic genome of Escherichia coli
Abstract
An approximation to the ~4-Mbp basic genome shared by 32 strains of E. coli representing six evolutionary groups has been derived and analyzed computationally. A multiple-alignment of the 32 complete genome sequences was filtered to remove mobile elements and identify the most reliable ~90% of the aligned length of each of the resulting 496 basic-genome pairs. Patterns of single bp mutations (SNPs) in aligned pairs distinguish clonally inherited regions from regions where either genome has acquired DNA fragments from diverged genomes by homologous recombination since their last common ancestor. Such recombinant transfer is pervasive across the basic genome, mostly between genomes in the same evolutionary group, and generates many unique mosaic patterns. The six least-diverged genome-pairs have one or two recombinant transfers of length ~40–115 kbp (and few if any other transfers), each containing one or more gene clusters known to confer strong selective advantage in some environments. Moderately diverged genome pairs (0.4–1% SNPs) show mosaic patterns of interspersed clonal and recombinant regions of varying lengths throughout the basic genome, whereas more highly diverged pairs within an evolutionary group or pairs between evolutionary groups having >1.3% SNPs have few clonal matches longer than a few kbp. Many recombinant transfers appearmore »
- Authors:
-
- Biological, Environmental and Climate Sciences Department, Brookhaven National Laboratory, Upton, NY 11973
- Publication Date:
- Research Org.:
- Brookhaven National Laboratory (BNL), Upton, NY (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1235129
- Alternate Identifier(s):
- OSTI ID: 1214531
- Report Number(s):
- BNL-108341-2015-JA
Journal ID: ISSN 0027-8424
- Grant/Contract Number:
- PM-031; ELS165; Internal research funding; SC00112704
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 29; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; E. coli evolution; basic genome; core genome; recombinant transfer; generalized transduction
Citation Formats
Dixit, Purushottam D., Pang, Tin Yau, Studier, F. William, and Maslov, Sergei. Recombinant transfer in the basic genome of Escherichia coli. United States: N. p., 2015.
Web. doi:10.1073/pnas.1510839112.
Dixit, Purushottam D., Pang, Tin Yau, Studier, F. William, & Maslov, Sergei. Recombinant transfer in the basic genome of Escherichia coli. United States. https://doi.org/10.1073/pnas.1510839112
Dixit, Purushottam D., Pang, Tin Yau, Studier, F. William, and Maslov, Sergei. Tue .
"Recombinant transfer in the basic genome of Escherichia coli". United States. https://doi.org/10.1073/pnas.1510839112.
@article{osti_1235129,
title = {Recombinant transfer in the basic genome of Escherichia coli},
author = {Dixit, Purushottam D. and Pang, Tin Yau and Studier, F. William and Maslov, Sergei},
abstractNote = {An approximation to the ~4-Mbp basic genome shared by 32 strains of E. coli representing six evolutionary groups has been derived and analyzed computationally. A multiple-alignment of the 32 complete genome sequences was filtered to remove mobile elements and identify the most reliable ~90% of the aligned length of each of the resulting 496 basic-genome pairs. Patterns of single bp mutations (SNPs) in aligned pairs distinguish clonally inherited regions from regions where either genome has acquired DNA fragments from diverged genomes by homologous recombination since their last common ancestor. Such recombinant transfer is pervasive across the basic genome, mostly between genomes in the same evolutionary group, and generates many unique mosaic patterns. The six least-diverged genome-pairs have one or two recombinant transfers of length ~40–115 kbp (and few if any other transfers), each containing one or more gene clusters known to confer strong selective advantage in some environments. Moderately diverged genome pairs (0.4–1% SNPs) show mosaic patterns of interspersed clonal and recombinant regions of varying lengths throughout the basic genome, whereas more highly diverged pairs within an evolutionary group or pairs between evolutionary groups having >1.3% SNPs have few clonal matches longer than a few kbp. Many recombinant transfers appear to incorporate fragments of the entering DNA produced by restriction systems of the recipient cell. A simple computational model can closely fit the data. As a result, most recombinant transfers seem likely to be due to generalized transduction by co-evolving populations of phages, which could efficiently distribute variability throughout bacterial genomes.},
doi = {10.1073/pnas.1510839112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 29,
volume = 112,
place = {United States},
year = {Tue Jul 07 00:00:00 EDT 2015},
month = {Tue Jul 07 00:00:00 EDT 2015}
}
https://doi.org/10.1073/pnas.1510839112
Web of Science
Works referenced in this record:
Horizontal gene transfer, genome innovation and evolution
journal, August 2005
- Gogarten, J. Peter; Townsend, Jeffrey P.
- Nature Reviews Microbiology, Vol. 3, Issue 9
Mutation Rate Inferred From Synonymous Substitutions in a Long-Term Evolution Experiment With Escherichia coli
journal, August 2011
- Wielgoss, Sébastien; Barrick, Jeffrey E.; Tenaillon, Olivier
- G3: Genes|Genomes|Genetics, Vol. 1, Issue 3
Lateral gene transfer and the nature of bacterial innovation
journal, May 2000
- Ochman, Howard; Lawrence, Jeffrey G.; Groisman, Eduardo A.
- Nature, Vol. 405, Issue 6784
Recombination in Escherichia coli and the definition of biological species.
journal, November 1991
- Dykhuizen, D. E.; Green, L.
- Journal of Bacteriology, Vol. 173, Issue 22
Molecular Evolution of the Escherichia coli Chromosome. VI. Two Regions of High Effective Recombination
journal, February 2003
- Milkman, Roger; Jaeger, Erich; McBride, Ryan D.
- Genetics, Vol. 163, Issue 2
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
Explaining microbial population genomics through phage predation
journal, November 2009
- Rodriguez-Valera, Francisco; Martin-Cuadrado, Ana-Belen; Rodriguez-Brito, Beltran
- Nature Reviews Microbiology, Vol. 7, Issue 11
Molecular keys to speciation: DNA polymorphism and the control of genetic exchange in enterobacteria
journal, September 1997
- Vulic, M.; Dionisio, F.; Taddei, F.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 18
Origins of the Coalescent: 1974-1982
journal, December 2000
- Kingman, J. F. C.
- Genetics, Vol. 156, Issue 4
A generalized transducing phage for the murine pathogen Citrobacter rodentium
journal, September 2007
- Petty, N. K.; Toribio, A. L.; Goulding, D.
- Microbiology, Vol. 153, Issue 9
Cassette-like variation of restriction enzyme genes in Escherichia coli C and relatives
journal, January 2004
- Sibley, M. H.
- Nucleic Acids Research, Vol. 32, Issue 2
The population genetics of commensal Escherichia coli
journal, March 2010
- Tenaillon, Olivier; Skurnik, David; Picard, Bertrand
- Nature Reviews Microbiology, Vol. 8, Issue 3
Transduction, restriction and recombination patterns in Escherichia coli.
journal, January 1995
- McKane, M.; Milkman, R.
- Genetics, Vol. 139, Issue 1
Clonal divergence in Escherichia coli as a result of recombination, not mutation
journal, November 1994
- Guttman, D.; Dykhuizen, D.
- Science, Vol. 266, Issue 5189
Understanding the Differences between Genome Sequences of Escherichia coli B Strains REL606 and BL21(DE3) and Comparison of the E. coli B and K-12 Genomes
journal, December 2009
- Studier, F. William; Daegelen, Patrick; Lenski, Richard E.
- Journal of Molecular Biology, Vol. 394, Issue 4
Prokaryotic Evolution in Light of Gene Transfer
journal, December 2002
- Gogarten, J. Peter; Doolittle, W. Ford; Lawrence, Jeffrey G.
- Molecular Biology and Evolution, Vol. 19, Issue 12
Estimating the size of the bacterial pan-genome
journal, March 2009
- Lapierre, Pascal; Gogarten, J. Peter
- Trends in Genetics, Vol. 25, Issue 3
The Evolutionary Path to Extraintestinal Pathogenic, Drug-Resistant Escherichia coli Is Marked by Drastic Reduction in Detectable Recombination within the Core Genome
journal, March 2013
- McNally, Alan; Cheng, Lu; Harris, Simon R.
- Genome Biology and Evolution, Vol. 5, Issue 4
Highlights of the DNA cutters: a short history of the restriction enzymes
journal, October 2013
- Loenen, Wil A. M.; Dryden, David T. F.; Raleigh, Elisabeth A.
- Nucleic Acids Research, Vol. 42, Issue 1
Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli
journal, June 2008
- Blount, Z. D.; Borland, C. Z.; Lenski, R. E.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 23
Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths
journal, January 2009
- Touchon, Marie; Hoede, Claire; Tenaillon, Olivier
- PLoS Genetics, Vol. 5, Issue 1
Mutation, recombination, and incipient speciation of bacteria in the laboratory
journal, June 1999
- Vulic, M.; Lenski, R. E.; Radman, M.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 13
Horizontal gene transfer and the evolution of bacterial and archaeal population structure
journal, March 2013
- Polz, Martin F.; Alm, Eric J.; Hanage, William P.
- Trends in Genetics, Vol. 29, Issue 3
Barriers to Genetic Exchange between Bacterial Species: Streptococcus pneumoniae Transformation
journal, February 2000
- Majewski, J.; Zawadzki, P.; Pickerill, P.
- Journal of Bacteriology, Vol. 182, Issue 4
The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust.
journal, July 1995
- Zawadzki, P.; Roberts, M. S.; Cohan, F. M.
- Genetics, Vol. 140, Issue 3
Bacteriophages and genetic mobilization in sewage and faecally polluted environments: Phages and faecal environments
journal, April 2011
- Muniesa, Maite; Imamovic, Lejla; Jofre, Juan
- Microbial Biotechnology, Vol. 4, Issue 6
Recombination and Population Structure in Escherichia coli
journal, July 1997
- Milkman, Roger
- Genetics, Vol. 146, Issue 3
Insertion Sequences
journal, September 1998
- Mahillon, Jacques; Chandler, Michael
- Microbiology and Molecular Biology Reviews, Vol. 62, Issue 3
Genome-wide detection and analysis of homologous recombination among sequenced strains of Escherichia coli
journal, January 2006
- Mau, Bob; Glasner, Jeremy D.; Darling, Aaron E.
- Genome Biology, Vol. 7, Issue 5, p. R44
Inferring Coalescence Times From DNA Sequence Data
journal, February 1997
- Tavaré, Simon; Balding, David J.; Griffiths, R. C.
- Genetics, Vol. 145, Issue 2
Pervasive domestication of defective prophages by bacteria
journal, August 2014
- Bobay, L. -M.; Touchon, M.; Rocha, E. P. C.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 33
The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity
journal, February 2009
- Fraser, C.; Alm, E. J.; Polz, M. F.
- Science, Vol. 323, Issue 5915
Recombination and the Nature of Bacterial Speciation
journal, January 2007
- Fraser, C.; Hanage, W. P.; Spratt, B. G.
- Science, Vol. 315, Issue 5811
Type I restriction enzymes and their relatives
journal, September 2013
- Loenen, W. A. M.; Dryden, D. T. F.; Raleigh, E. A.
- Nucleic Acids Research, Vol. 42, Issue 1
Inference of the Properties of the Recombination Process from Whole Bacterial Genomes
journal, October 2013
- Ansari, M. Azim; Didelot, Xavier
- Genetics, Vol. 196, Issue 1
Isolation of Generalized Transducing Bacteriophages for Uropathogenic Strains of Escherichia coli
journal, July 2011
- Battaglioli, E. J.; Baisa, G. A.; Weeks, A. E.
- Applied and Environmental Microbiology, Vol. 77, Issue 18
Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches
journal, September 2011
- Wiedenbeck, Jane; Cohan, Frederick M.
- FEMS Microbiology Reviews, Vol. 35, Issue 5
Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli
journal, January 2012
- Didelot, Xavier; Méric, Guillaume; Falush, Daniel
- BMC Genomics, Vol. 13, Issue 1
Molecular Evolution of the Escherichia coli Chromosome. V. Recombination Patterns Among Strains of Diverse Origin
journal, October 1999
- Milkman, Roger; Raleigh, Elisabeth A.; McKane, Melissa
- Genetics, Vol. 153, Issue 2