XerD is required to unload bacterial SMC complexes at the replication terminus

Bacillus subtilis SMC complexes are topologically loaded at centromeric sites adjacent to the replication origin by the partitioning protein ParB. These ring-shaped ATPases then translocate down the left and right chromosome arms while tethering them together. Here we show that the site-specific recombinase XerD that resolves chromosome dimers is required to unload SMC tethers when they reach the terminus. We identify XerD-specific binding sites in the terminus region and show that they dictate the site of unloading in a manner that depends on XerD but not its catalytic residue, its partner protein XerC, or the recombination site dif. Finally, we provide evidence that ParB and XerD homologs perform similar functions in Staphylococcus aureus. Thus, loading and unloading of SMC complexes are mediated by two broadly conserved factors: one involved in origin segregation, the other in terminus resolution. Similar site-specific unloading activities could modulate eukaryotic SMC complexes during interphase and mitosis. Hi-C and ChIP-seq experiments were performed on wild type and mutant cells of Bacillus subtilis PY79 and Staphylococcus aureus HG003 growing in rich media.