Parallel Compensatory Evolution Stabilizes Plasmids across the Parasitism-Mutualism Continuum

Horizontal Gene Transfer Mutualism Gene transfer
DOI: 10.1016/j.cub.2015.06.024 Publication Date: 2015-07-17T05:30:46Z
ABSTRACT
Plasmids drive genomic diversity in bacteria via horizontal gene transfer [1Thomas C.M. Nielsen K.M. Mechanisms of, and barriers to, between bacteria.Nat. Rev. Microbiol. 2005; 3: 711-721Crossref PubMed Scopus (1283) Google Scholar, 2Jain R. Rivera M.C. Moore J.E. Lake J.A. Horizontal accelerates genome innovation evolution.Mol. Biol. Evol. 2003; 20: 1598-1602Crossref (242) Scholar]; nevertheless, explaining their survival bacterial populations is challenging [3Harrison E. Brockhurst M.A. Plasmid-mediated a coevolutionary process.Trends 2012; 262-267Abstract Full Text PDF (194) Scholar]. Theory predicts that irrespective of net fitness effects, plasmids should be lost: when parasitic (costs outweigh benefits), decline due to purifying selection [4Bergstrom C.T. Lipsitch M. Levin B.R. Natural selection, infectious the existence conditions for plasmids.Genetics. 2000; 155: 1505-1519PubMed 5Levin The accessory genetic elements bacteria: (co)evolution.Curr. Opin. Genet. Dev. 1993; 849-854Crossref (29) 6Sørensen S.J. Bailey Hansen L.H. Kroer N. Wuertz S. Studying plasmid situ: critical review.Nat. 700-710Crossref (498) Scholar], yet under mutualism (benefits costs), favors capture beneficial genes by chromosome loss costly backbone While compensatory evolution can enhance stability within [7Bouma Lenski R.E. Evolution bacteria/plasmid association.Nature. 1988; 335: 351-352Crossref (332) 8San Millan A. Peña-Miller Toll-Riera Halbert Z.V. McLean A.R. Cooper B.S. MacLean R.C. Positive adaptation interact stabilize non-transmissible plasmids.Nat. Commun. 2014; 5: 5208Crossref (143) 9Dahlberg C. Chao L. Amelioration cost conjugative carriage Eschericha coli K12.Genetics. 165: 1641-1649PubMed 10Dionisio F. Conceição I.C. Marques A.C.R. Fernandes Gordo I. its ability increase fitness.Biol. Lett. 1: 250-252Crossref (122) 11Modi R.I. Adams J. Coevolution - populations.Evolution. 1991; 45: 656-667Crossref 12Modi Wilke Rosenzweig R.F. Plasmid macro-evolution: deletions during nutrient-limited environment.Genetica. 84: 195-202Crossref (37) 13San Santos-Lopez Ortega Huedo Bernabe-Balas Kennedy S.P. Gonzalez-Zorn B. Small-plasmid-mediated antibiotic resistance enhanced increases copy number fitness.Antimicrob. Agents Chemother. 2015; 59: 3335-3341Crossref (43) 14Hughes J.M. Lohman B.K. Deckert G.E. Nichols E.P. Settles Abdo Z. Top E.M. role clonal interference evolutionary dynamics plasmid-host adaptation.MBio. 3 (e00077–e12)Crossref (28) 15San Qi Q. Interactions horizontally acquired create Pseudomonas aeruginosa.Nat. 6: 6845Crossref (102) propensity this occur across parasitism-mutualism continuum unknown. We experimentally evolved fluorescens mercury mega-plasmid, pQBR103 [16Tett Spiers A.J. Crossman L.C. Ager D. Ciric Dow Fry J.C. Harris Lilley Oliver et al.Sequence-based analysis pQBR103; representative unique, transfer-proficient mega resident microbial community sugar beet.ISME 2007; 331-340PubMed an environment-mediated continuum. Compensatory stabilized rapidly ameliorating all environments. Genomic revealed that, both mutualistic treatments, repeatedly targeted gacA/gacS two-component global regulatory system while leaving sequence intact. Deletion either gacA or gacS was sufficient completely ameliorate carriage. Mutation downregulated expression ∼17% chromosomal appears have relieved translational demand imposed plasmid. Chromosomal accompanied occurred throughout experiment but very rarely invaded high frequency, suggesting rapid limit process. explain widespread occurrence allows retain even environments where are not immediately useful.
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