Literature DB >> 28646326

Transposable Elements Mediate Adaptive Debilitation of Flagella in Experimental Escherichia coli Populations.

Gordon R Plague1, Krystal S Boodram2, Kevin M Dougherty3, Sandar Bregg4,5, Daniel P Gilbert4,6, Hira Bakshi4, Daniel Costa4,7.   

Abstract

Although insertion sequence (IS) elements are generally considered genomic parasites, they can mediate adaptive genetic changes in bacterial genomes. We discovered that among 12 laboratory-evolved Escherichia coli populations, three had experienced at least six different IS1-mediated deletions of flagellar genes. These deletions all involved the master flagellar regulator flhDC, and as such completely incapacitate motility. Two lines of evidence strongly suggest that these deletions were adaptive in our evolution experiment: (1) parallel evolution in three independent populations is highly unlikely just by chance, and (2) one of these deletion mutations swept to fixation within ~1000 generations, which is over two million times faster than expected if this deletion was instead selectively neutral and thus evolving by genetic drift. Because flagella are energetically expensive to synthesize and operate, we suspect that debilitating their construction conferred a fitness advantage in our well-stirred evolution experiment. These findings underscore the important role that IS elements can play in mediating adaptive loss-of-function mutations in bacteria.

Entities:  

Keywords:  Adaptive evolution; Experimental evolution; Insertion sequence element; Loss-of-function mutation; Natural selection; Parallel evolution

Mesh:

Substances:

Year:  2017        PMID: 28646326      PMCID: PMC6002858          DOI: 10.1007/s00239-017-9797-5

Source DB:  PubMed          Journal:  J Mol Evol        ISSN: 0022-2844            Impact factor:   2.395


  38 in total

1.  Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica.

Authors:  Julian Parkhill; Mohammed Sebaihia; Andrew Preston; Lee D Murphy; Nicholas Thomson; David E Harris; Matthew T G Holden; Carol M Churcher; Stephen D Bentley; Karen L Mungall; Ana M Cerdeño-Tárraga; Louise Temple; Keith James; Barbara Harris; Michael A Quail; Mark Achtman; Rebecca Atkin; Steven Baker; David Basham; Nathalie Bason; Inna Cherevach; Tracey Chillingworth; Matthew Collins; Anne Cronin; Paul Davis; Jonathan Doggett; Theresa Feltwell; Arlette Goble; Nancy Hamlin; Heidi Hauser; Simon Holroyd; Kay Jagels; Sampsa Leather; Sharon Moule; Halina Norberczak; Susan O'Neil; Doug Ormond; Claire Price; Ester Rabbinowitsch; Simon Rutter; Mandy Sanders; David Saunders; Katherine Seeger; Sarah Sharp; Mark Simmonds; Jason Skelton; Robert Squares; Steven Squares; Kim Stevens; Louise Unwin; Sally Whitehead; Bart G Barrell; Duncan J Maskell
Journal:  Nat Genet       Date:  2003-08-10       Impact factor: 38.330

2.  Insertion-sequence-mediated mutations isolated during adaptation to growth and starvation in Lactococcus lactis.

Authors:  J Arjan G M de Visser; Antoon D L Akkermans; Rolf F Hoekstra; Willem M de Vos
Journal:  Genetics       Date:  2004-11       Impact factor: 4.562

Review 3.  The genetic causes of convergent evolution.

Authors:  David L Stern
Journal:  Nat Rev Genet       Date:  2013-10-09       Impact factor: 53.242

4.  Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli.

Authors:  D S Treves; S Manning; J Adams
Journal:  Mol Biol Evol       Date:  1998-07       Impact factor: 16.240

5.  The complete genome sequence of Escherichia coli K-12.

Authors:  F R Blattner; G Plunkett; C A Bloch; N T Perna; V Burland; M Riley; J Collado-Vides; J D Glasner; C K Rode; G F Mayhew; J Gregor; N W Davis; H A Kirkpatrick; M A Goeden; D J Rose; B Mau; Y Shao
Journal:  Science       Date:  1997-09-05       Impact factor: 47.728

6.  Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements.

Authors:  J A Shapiro
Journal:  Proc Natl Acad Sci U S A       Date:  1979-04       Impact factor: 11.205

7.  Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing.

Authors:  Heewook Lee; Ellen Popodi; Haixu Tang; Patricia L Foster
Journal:  Proc Natl Acad Sci U S A       Date:  2012-09-18       Impact factor: 11.205

8.  A simple method for genome-wide screening for advantageous insertions of mobile DNAs in Escherichia coli.

Authors:  Richard J Edwards; R Elizabeth Sockett; John F Y Brookfield
Journal:  Curr Biol       Date:  2002-05-14       Impact factor: 10.834

9.  Insertion sequence-driven evolution of Escherichia coli in chemostats.

Authors:  Joël Gaffé; Christopher McKenzie; Ram P Maharjan; Evelyne Coursange; Tom Ferenci; Dominique Schneider
Journal:  J Mol Evol       Date:  2011-03-12       Impact factor: 2.395

10.  Evolutionary genomics of ecological specialization.

Authors:  Shaobin Zhong; Arkady Khodursky; Daniel E Dykhuizen; Antony M Dean
Journal:  Proc Natl Acad Sci U S A       Date:  2004-08-02       Impact factor: 11.205

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  1 in total

1.  Exploring the fitness benefits of genome reduction in Escherichia coli by a selection-driven approach.

Authors:  Viktor Vernyik; Ildikó Karcagi; Edit Tímár; István Nagy; Ádám Györkei; Balázs Papp; Zsuzsanna Györfy; György Pósfai
Journal:  Sci Rep       Date:  2020-04-30       Impact factor: 4.379

  1 in total

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