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Title: Recombinant transfer in the basic genome of E. 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 » 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.« less

Authors:
 [1];  [2];  [3];  [4]
  1. Brookhaven National Lab. (BNL), Upton, NY (United States); Columbia Univ., New York, NY (United States)
  2. Brookhaven National Lab. (BNL), Upton, NY (United States)
  3. Brookhaven National Lab. (BNL), Upton, NY (United States); Heinrich-Heine-Univ. Dusseldorf Univ., Dusseldorf (Germany)
  4. Brookhaven National Lab. (BNL), Upton, NY (United States); Univ. of Illinois at Urbana-Champaign, Urbana, IL (United States)
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1235129
Alternate Identifier(s):
OSTI ID: 1214531
Report Number(s):
BNL-108341-2015-JA
Journal ID: ISSN 0027-8424; R&D Project: PM-031; ELS-165; KP1601040
Grant/Contract Number:  
SC00112704; PM-031; ELS165; Internal research funding
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 29; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
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, Studier, F. William, Pang, Tin Yau, and Maslov, Sergei. Recombinant transfer in the basic genome of E. coli. United States: N. p., 2015. Web. doi:10.1073/pnas.1510839112.
Dixit, Purushottam, Studier, F. William, Pang, Tin Yau, & Maslov, Sergei. Recombinant transfer in the basic genome of E. coli. United States. doi:10.1073/pnas.1510839112.
Dixit, Purushottam, Studier, F. William, Pang, Tin Yau, and Maslov, Sergei. Tue . "Recombinant transfer in the basic genome of E. coli". United States. doi:10.1073/pnas.1510839112.
@article{osti_1235129,
title = {Recombinant transfer in the basic genome of E. coli},
author = {Dixit, Purushottam and Studier, F. William and Pang, Tin Yau 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 = {2015},
month = {7}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1510839112

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Cited by: 19 works
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Works referenced in this record:

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
  • DOI: 10.1038/35012500

Horizontal gene transfer, genome innovation and evolution
journal, August 2005

  • Gogarten, J. Peter; Townsend, Jeffrey P.
  • Nature Reviews Microbiology, Vol. 3, Issue 9
  • DOI: 10.1038/nrmicro1204

Recombination and the Nature of Bacterial Speciation
journal, January 2007


The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity
journal, February 2009


Estimating the size of the bacterial pan-genome
journal, March 2009


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
  • DOI: 10.1038/nrmicro2235

Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches
journal, September 2011


Horizontal gene transfer and the evolution of bacterial and archaeal population structure
journal, March 2013


The population genetics of commensal Escherichia coli
journal, March 2010

  • Tenaillon, Olivier; Skurnik, David; Picard, Bertrand
  • Nature Reviews Microbiology, Vol. 8, Issue 3
  • DOI: 10.1038/nrmicro2298

Prokaryotic Evolution in Light of Gene Transfer
journal, December 2002


Organised Genome Dynamics in the Escherichia coli Species Results in Highly Diverse Adaptive Paths
journal, January 2009


Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli
journal, January 2012


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
  • DOI: 10.1073/pnas.0803151105

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
  • DOI: 10.1073/pnas.96.13.7348

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
  • DOI: 10.1073/pnas.1405336111

Recombination in Escherichia coli and the definition of biological species.
journal, November 1991


Clonal divergence in Escherichia coli as a result of recombination, not mutation
journal, November 1994


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
  • DOI: 10.1016/j.jmb.2009.09.021

progressiveMauve: Multiple Genome Alignment with Gene Gain, Loss and Rearrangement
journal, June 2010


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
  • DOI: 10.1534/g3.111.000406

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
  • DOI: 10.1093/nar/gkt847

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
  • DOI: 10.1093/nar/gkt990

Cassette-like variation of restriction enzyme genes in Escherichia coli C and relatives
journal, January 2004


Bacteriophages and genetic mobilization in sewage and faecally polluted environments: Phages and faecal environments
journal, April 2011


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
  • DOI: 10.1128/AEM.05307-11

A generalized transducing phage for the murine pathogen Citrobacter rodentium
journal, September 2007


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
  • DOI: 10.1073/pnas.94.18.9763

Barriers to Genetic Exchange between Bacterial Species: Streptococcus pneumoniae Transformation
journal, February 2000


Inference of the Properties of the Recombination Process from Whole Bacterial Genomes
journal, October 2013


    Works referencing / citing this record:

    Benefit of transferred mutations is better predicted by the fitness of recipients than by their ecological or genetic relatedness
    journal, April 2016

    • Wang, Yinhua; Diaz Arenas, Carolina; Stoebel, Daniel M.
    • Proceedings of the National Academy of Sciences, Vol. 113, Issue 18
    • DOI: 10.1073/pnas.1524988113

    Mutator genomes decay, despite sustained fitness gains, in a long-term experiment with bacteria
    journal, October 2017

    • Couce, Alejandro; Caudwell, Larissa Viraphong; Feinauer, Christoph
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 43
    • DOI: 10.1073/pnas.1705887114

    Synonymous Genetic Variation in Natural Isolates of Escherichia coli Does Not Predict Where Synonymous Substitutions Occur in a Long-Term Experiment
    journal, July 2015

    • Maddamsetti, Rohan; Hatcher, Philip J.; Cruveiller, Stéphane
    • Molecular Biology and Evolution, Vol. 32, Issue 11
    • DOI: 10.1093/molbev/msv161

    Pandemic fluoroquinolone resistant Escherichia coli clone ST1193 emerged via simultaneous homologous recombinations in 11 gene loci
    journal, July 2019

    • Tchesnokova, Veronika; Radey, Matthew; Chattopadhyay, Sujay
    • Proceedings of the National Academy of Sciences, Vol. 116, Issue 29
    • DOI: 10.1073/pnas.1903002116