Literature DB >> 20083614

Duplication frequency in a population of Salmonella enterica rapidly approaches steady state with or without recombination.

Andrew B Reams1, Eric Kofoid, Michael Savageau, John R Roth.   

Abstract

Tandem duplications are among the most common mutation events. The high loss rate of duplication suggested that the frequency of duplications in a bacterial population (1/1000) might reflect a steady state dictated by relative rates of formation (k(F)) and loss (k(L)). This possibility was tested for three genetic loci. Without homologous recombination (RecA), duplication loss rate dropped essentially to zero, but formation rate decreased only slightly and a steady state was still reached rapidly. Under all conditions, steady state was reached faster than predicted by formation and loss rates alone. A major factor in determining steady state proved to be the fitness cost, which can exceed 40% for some genomic regions. Depending on the region tested, duplications reached 40-98% of the steady-state frequency within 30 generations-approximately the growth required for a single cell to produce a saturated overnight culture or form a large colony on solid medium (10(9) cells). Long-term bacterial populations are stably polymorphic for duplications of every region of their genome. These polymorphisms contribute to rapid genetic adaptation by providing frequent preexisting mutations that are beneficial whenever imposed selection favors increases in some gene activity. While the reported results were obtained with the bacterium Salmonella enterica, the genetic implications seem likely to be of broader biological relevance.

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Year:  2010        PMID: 20083614      PMCID: PMC2865909          DOI: 10.1534/genetics.109.111963

Source DB:  PubMed          Journal:  Genetics        ISSN: 0016-6731            Impact factor:   4.562


  32 in total

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Authors:  S Bachellier; J M Clément; M Hofnung
Journal:  Res Microbiol       Date:  1999 Nov-Dec       Impact factor: 3.992

2.  Recombineering with overlapping single-stranded DNA oligonucleotides: testing a recombination intermediate.

Authors:  Daiguan Yu; James A Sawitzke; Hilary Ellis; Donald L Court
Journal:  Proc Natl Acad Sci U S A       Date:  2003-05-27       Impact factor: 11.205

3.  Adaptive mutation: general mutagenesis is not a programmed response to stress but results from rare coamplification of dinB with lac.

Authors:  E Susan Slechta; Kim L Bunny; Elisabeth Kugelberg; Eric Kofoid; Dan I Andersson; John R Roth
Journal:  Proc Natl Acad Sci U S A       Date:  2003-10-14       Impact factor: 11.205

4.  Gene duplication in bacteria: alteration of gene dosage by sister-chromosome exchanges.

Authors:  R P Anderson; J R Roth
Journal:  Cold Spring Harb Symp Quant Biol       Date:  1979

Review 5.  Tandem genetic duplications in phage and bacteria.

Authors:  R P Anderson; J R Roth
Journal:  Annu Rev Microbiol       Date:  1977       Impact factor: 15.500

Review 6.  Genetic engineering using homologous recombination.

Authors:  Donald L Court; James A Sawitzke; Lynn C Thomason
Journal:  Annu Rev Genet       Date:  2002-06-11       Impact factor: 16.830

7.  Production of extrachromosomal r-determinant circles from integrated R100.1: involvement of the E. coli recombination system.

Authors:  L Silver; M Chandler; H E Lane; L Caro
Journal:  Mol Gen Genet       Date:  1980

8.  Formation of an F' plasmid by recombination between imperfectly repeated chromosomal Rep sequences: a closer look at an old friend (F'(128) pro lac).

Authors:  Eric Kofoid; Ulfar Bergthorsson; E Susan Slechta; John R Roth
Journal:  J Bacteriol       Date:  2003-01       Impact factor: 3.490

9.  Origins and functional impact of copy number variation in the human genome.

Authors:  Donald F Conrad; Dalila Pinto; Richard Redon; Lars Feuk; Omer Gokcumen; Yujun Zhang; Jan Aerts; T Daniel Andrews; Chris Barnes; Peter Campbell; Tomas Fitzgerald; Min Hu; Chun Hwa Ihm; Kati Kristiansson; Daniel G Macarthur; Jeffrey R Macdonald; Ifejinelo Onyiah; Andy Wing Chun Pang; Sam Robson; Kathy Stirrups; Armand Valsesia; Klaudia Walter; John Wei; Chris Tyler-Smith; Nigel P Carter; Charles Lee; Stephen W Scherer; Matthew E Hurles
Journal:  Nature       Date:  2009-10-07       Impact factor: 49.962

10.  Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons.

Authors:  P Anderson; J Roth
Journal:  Proc Natl Acad Sci U S A       Date:  1981-05       Impact factor: 11.205

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  63 in total

1.  Dynamics of gene duplication and transposons in microbial genomes following a sudden environmental change.

Authors:  Nicholas Chia; Nicholas Guttenberg
Journal:  Mob Genet Elements       Date:  2011-09-01

Review 2.  Toward a systems biology perspective on enzyme evolution.

Authors:  Shelley D Copley
Journal:  J Biol Chem       Date:  2011-11-08       Impact factor: 5.157

3.  The joys and terrors of fast adaptation: new findings elucidate antibiotic resistance and natural selection.

Authors:  John R Roth
Journal:  Mol Microbiol       Date:  2010-11-21       Impact factor: 3.501

4.  Reinterpreting Long-Term Evolution Experiments: Is Delayed Adaptation an Example of Historical Contingency or a Consequence of Intermittent Selection?

Authors:  John R Roth; Sophie Maisnier-Patin
Journal:  J Bacteriol       Date:  2016-02-16       Impact factor: 3.490

5.  Amplification of the gene for isoleucyl-tRNA synthetase facilitates adaptation to the fitness cost of mupirocin resistance in Salmonella enterica.

Authors:  Wilhelm Paulander; Dan I Andersson; Sophie Maisnier-Patin
Journal:  Genetics       Date:  2010-02-22       Impact factor: 4.562

6.  Fitness effects of replichore imbalance in Salmonella enterica.

Authors:  T David Matthews; Stanley Maloy
Journal:  J Bacteriol       Date:  2010-09-24       Impact factor: 3.490

7.  Molecular mechanisms of multiple toxin-antitoxin systems are coordinated to govern the persister phenotype.

Authors:  Rick A Fasani; Michael A Savageau
Journal:  Proc Natl Acad Sci U S A       Date:  2013-06-18       Impact factor: 11.205

8.  Recombination and annealing pathways compete for substrates in making rrn duplications in Salmonella enterica.

Authors:  Andrew B Reams; Eric Kofoid; Natalie Duleba; John R Roth
Journal:  Genetics       Date:  2013-11-08       Impact factor: 4.562

9.  Selection-Enhanced Mutagenesis of lac Genes Is Due to Their Coamplification with dinB Encoding an Error-Prone DNA Polymerase.

Authors:  Itsugo Yamayoshi; Sophie Maisnier-Patin; John R Roth
Journal:  Genetics       Date:  2018-01-04       Impact factor: 4.562

10.  The birth of a bacterial tRNA gene by large-scale, tandem duplication events.

Authors:  Gökçe B Ayan; Hye Jin Park; Jenna Gallie
Journal:  Elife       Date:  2020-10-30       Impact factor: 8.140

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