Originally published as Genetics Published Articles Ahead of Print on April 3, 2007.

Genetics, Vol. 176, 513-526, May 2007, Copyright © 2007
doi:10.1534/genetics.106.056150

Evolution of DNA Double-Strand Break Repair by Gene Conversion: Coevolution Between a Phage and a Restriction-Modification System

Koji Yahara^*, Ryota Horie, Ichizo Kobayashi^*,,1 and Akira Sasaki^,**

^* Laboratory of Social Genome Sciences, Department of Medical Genome Sciences, Graduate School of Frontier Science and Institute of Medical Science and Graduate Program of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, Tokyo 108-8639, Japan, Laboratory for Language Development, RIKEN Brain Science Institute, Saitama 351-0198, Japan, Department of Biology, Faculty of Sciences, Kyushu University, Fukuoka 812-8581, Japan and ^** Evolution and Ecology Program, International Institute for Applied Systems Analysis, A-2361 Laxenburg, Austria

¹ Corresponding author: Laboratory of Social Genome Sciences, Department of Medical Genome Sciences, Graduate School of Frontier Science and Institute of Medical Science, University of Tokyo, 4-6-1 Shirokanedai, Minato-ku, Tokyo 108-8639, Japan.
E-mail: ikobaya{at}ims.u-tokyo.ac.jp

The necessity to repair genome damage has been considered to be an immediate factor responsible for the origin of sex. Indeed, attack by a cellular restriction enzyme of invading DNA from several bacteriophages initiates recombinational repair by gene conversion if there is homologous DNA. In this work, we modeled the interaction between a bacteriophage and a bacterium carrying a restriction enzyme as antagonistic coevolution. We assume a locus on the bacteriophage genome has either a restriction-sensitive or a restriction-resistant allele, and another locus determines whether it is recombination/repair proficient or defective. A restriction break can be repaired by a co-infecting phage genome if one of them is recombination/repair proficient. We define the fitness of phage (resistant/sensitive and repair-positive/-negative) genotypes and bacterial (restriction-positive/-negative) genotypes by assuming random encounter of the genotypes, with given probabilities of single and double infections, and the costs of resistance, repair, and restriction. Our results show the evolution of the repair allele depends on the ratio of the burst size under damage to host cell physiology induced by an unrepaired double-strand break to the default burst size It was not until this effect was taken into account that the evolutionary advantage of DNA repair became apparent.

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