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Selective Inbreeding: Genetic Crosses Drive Apparent Adaptive Mutation in the Cairns-Foster System of Escherichia coli.
Genetics. 2020 02; 214(2):333-354.G

Abstract

The Escherichia coli system of Cairns and Foster employs a lac frameshift mutation that reverts rarely (10-9/cell/division) during unrestricted growth. However, when 108 cells are plated on lactose medium, the nongrowing lawn produces ∼50 Lac+ revertant colonies that accumulate linearly with time over 5 days. Revertants carry very few associated mutations. This behavior has been attributed to an evolved mechanism ("adaptive mutation" or "stress-induced mutagenesis") that responds to starvation by preferentially creating mutations that improve growth. We describe an alternative model, "selective inbreeding," in which natural selection acts during intercellular transfer of the plasmid that carries the mutant lac allele and the dinB gene for an error-prone polymerase. Revertant genome sequences show that the plasmid is more intensely mutagenized than the chromosome. Revertants vary widely in their number of plasmid and chromosomal mutations. Plasmid mutations are distributed evenly, but chromosomal mutations are focused near the replication origin. Rare, heavily mutagenized, revertants have acquired a plasmid tra mutation that eliminates conjugation ability. These findings support the new model, in which revertants are initiated by rare pre-existing cells (105) with many copies of the F'lac plasmid. These cells divide under selection, producing daughters that mate. Recombination between donor and recipient plasmids initiates rolling-circle plasmid over-replication, causing a mutagenic elevation of DinB level. A lac+ reversion event starts chromosome replication and mutagenesis by accumulated DinB. After reversion, plasmid transfer moves the revertant lac+ allele into an unmutagenized cell, and away from associated mutations. Thus, natural selection explains why mutagenesis appears stress-induced and directed.

Authors+Show Affiliations

Department of Microbiology and Molecular Genetics, University of California, Davis, California 95616.Department of Microbiology and Molecular Genetics, University of California, Davis, California 95616 jrroth@ucdavis.edu smaisnierpatin@ucdavis.edu.Department of Microbiology and Molecular Genetics, University of California, Davis, California 95616.Department of Microbiology and Molecular Genetics, University of California, Davis, California 95616.Department of Microbiology and Molecular Genetics, University of California, Davis, California 95616 jrroth@ucdavis.edu smaisnierpatin@ucdavis.edu.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

31810989

Citation

Nguyen, Amanda, et al. "Selective Inbreeding: Genetic Crosses Drive Apparent Adaptive Mutation in the Cairns-Foster System of Escherichia Coli." Genetics, vol. 214, no. 2, 2020, pp. 333-354.
Nguyen A, Maisnier-Patin S, Yamayoshi I, et al. Selective Inbreeding: Genetic Crosses Drive Apparent Adaptive Mutation in the Cairns-Foster System of Escherichia coli. Genetics. 2020;214(2):333-354.
Nguyen, A., Maisnier-Patin, S., Yamayoshi, I., Kofoid, E., & Roth, J. R. (2020). Selective Inbreeding: Genetic Crosses Drive Apparent Adaptive Mutation in the Cairns-Foster System of Escherichia coli. Genetics, 214(2), 333-354. https://doi.org/10.1534/genetics.119.302754
Nguyen A, et al. Selective Inbreeding: Genetic Crosses Drive Apparent Adaptive Mutation in the Cairns-Foster System of Escherichia Coli. Genetics. 2020;214(2):333-354. PubMed PMID: 31810989.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Selective Inbreeding: Genetic Crosses Drive Apparent Adaptive Mutation in the Cairns-Foster System of Escherichia coli. AU - Nguyen,Amanda, AU - Maisnier-Patin,Sophie, AU - Yamayoshi,Itsugo, AU - Kofoid,Eric, AU - Roth,John R, Y1 - 2019/12/06/ PY - 2019/09/23/received PY - 2019/12/02/accepted PY - 2021/02/01/pmc-release PY - 2019/12/8/pubmed PY - 2019/12/8/medline PY - 2019/12/8/entrez KW - DNA repair KW - DinB KW - adaptive mutation KW - bacterial mating KW - break-induced replication KW - copy number variation KW - mutagenesis KW - plasmid transfer KW - recombination-dependent replication KW - rolling-circle replication KW - selection KW - selective gene amplification SP - 333 EP - 354 JF - Genetics JO - Genetics VL - 214 IS - 2 N2 - The Escherichia coli system of Cairns and Foster employs a lac frameshift mutation that reverts rarely (10-9/cell/division) during unrestricted growth. However, when 108 cells are plated on lactose medium, the nongrowing lawn produces ∼50 Lac+ revertant colonies that accumulate linearly with time over 5 days. Revertants carry very few associated mutations. This behavior has been attributed to an evolved mechanism ("adaptive mutation" or "stress-induced mutagenesis") that responds to starvation by preferentially creating mutations that improve growth. We describe an alternative model, "selective inbreeding," in which natural selection acts during intercellular transfer of the plasmid that carries the mutant lac allele and the dinB gene for an error-prone polymerase. Revertant genome sequences show that the plasmid is more intensely mutagenized than the chromosome. Revertants vary widely in their number of plasmid and chromosomal mutations. Plasmid mutations are distributed evenly, but chromosomal mutations are focused near the replication origin. Rare, heavily mutagenized, revertants have acquired a plasmid tra mutation that eliminates conjugation ability. These findings support the new model, in which revertants are initiated by rare pre-existing cells (105) with many copies of the F'lac plasmid. These cells divide under selection, producing daughters that mate. Recombination between donor and recipient plasmids initiates rolling-circle plasmid over-replication, causing a mutagenic elevation of DinB level. A lac+ reversion event starts chromosome replication and mutagenesis by accumulated DinB. After reversion, plasmid transfer moves the revertant lac+ allele into an unmutagenized cell, and away from associated mutations. Thus, natural selection explains why mutagenesis appears stress-induced and directed. SN - 1943-2631 UR - https://www.unboundmedicine.com/medline/citation/31810989/Selective_Inbreeding:_Genetic_Crosses_Drive_Apparent_Adaptive_Mutation_in_the_Cairns-Foster_System_of_Escherichia_coli L2 - http://www.genetics.org/cgi/pmidlookup?view=long&pmid=31810989 DB - PRIME DP - Unbound Medicine ER -
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