Hyperrecombination in the terminus region of the Escherichia coli chromosome: possible relation to nucleoid organization

Abstract

The terminus region of the Escherichia coli chromosome is the scene of frequent homologous recombination. This can be demonstrated by formation of deletions between directly repeated sequences which flank a genetic marker whose loss can be easily detected. We report here that terminal recombination events are restricted to a relatively large terminal recombination zone (TRZ). On one side of the TRZ, the transition from the region with a high excision rate to the normal (low) excision rates of the rest of the chromosome occurs along a DNA stretch of less than 1 min. No specific border of this domain has been defined. To identify factors inducing terminal recombination, we examined its relation to two other phenomena affecting the same region, site-specific recombination at the dif locus and site-specific replication pausing. Both the location and the efficiency of terminal recombination remained unchanged after inactivation of the dif-specific recombination system. Similarly, inactivation of site-specific replication pausing or displacement of the replication fork trap so that termination occurs about 200 kb away from the normal region had no clear effect on this phenomenon.Therefore, terminal recombination is not a direct consequence of either dif-specific recombination or replication termination. Furthermore, deletions encompassing the wild-type TRZ do not eliminate hyperrecombination. Terminal recombination therefore cannot be attributed to the activity of some unique sequence of the region. A possible explanation of terminal hyperrecombination involves nucleoid organization and its remodeling after replication: we propose that postreplicative reconstruction of the nucleoid organization results in a displacement of the catenation links between sister chromosomes to the last chromosomal domain to be rebuilt. Unrelated to replication termination, this process would facilitate interactions between the catenated molecules and would make the domain highly susceptible to recombination between sister chromosomes.The region of the Escherichia coli chromosome in which replication terminates is implicated in two recombination events occurring at high frequencies in cells with a wild-type cell cycle machinery. One is site-specific recombination, controlled by the XerCD recombinases (4), which takes place at a unique site, dif, located at 34 min on the genetic map (3,5,20).The dif-specific recombination probably participates in chromosome dimer resolution, since bacteria deleted for the dif locus, or made XerC-, have a tendency to form filaments (3,20), but the exact physiological role of dif-mediated recombination is not precisely known. The other very frequent event is homologous recombination between directly repeated sequences (24). The position where the phenomenon was the most striking (the zdd263::TnS locus) maps between dif and the first replication terminator acting on forks moving rightward in Fig. 1B, terC pothesis concerning the mechanism and the role for the hyperrecombination in the terminus region has been...

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