Inferences of organismal molecular evolution have been dominated by comparisons of their constituent genes. Yet the evolutionary histories of genes within Bacterial genomes are not necessarily congruent. Here, Horizontal Gene Transfer (HGT) of sequences across species boundaries can confound these analyses. There does appear to be phylogenetic cohesion, where members of higher taxonomic groups share genotypic similarity despite gene transfer. Herein I examine the rules for governing HGT to determine the impact this process has played in the evolution of Bacteria and Archaea. Bacterial chromosomes are more than simple lists of genes. Genomes must maintain information beyond component genes to direct efficient replication and segregation of their chromosomes. I propose that this structure constrains the process of HGT so that transfer among certain pairs of donors and recipients is favored. I present methods to detect this structure and new theories of bacterial cell biology and evolution based on what this structure reveals. I present evidence that bacterial chromosomes are structured by repetitive sequences termed Architecture IMparting Sequences (AIMS). AIMS are found primarily on leading strands and increase in abundance towards the replication terminus. Bacteria with robustly-identified replication origins and termini all have AIMS, and related AIMS are conserved amongst families of bacteria. We propose that AIMS are under selection to provide DNA binding proteins with polarity information, facilitating identification of the location of the replication terminus. Although AIMS evolved to direct the biology of cell division and replication, the conservation of AIMS among related taxa leads to a secondary effect. Because AIMS are counterselected when in nonpermissive orientations, AIMS constrain both intragenomic and intergenomic rearrangements. Thus HGT frequency will depend on AIMS compatibility between different species. We predict that HGT is most common between bacterial genomes which are more closely related and will impede transfer between species which have dissimilar genome architecture. The additional level of selection reflected by AIMS has resulted in cohesive bacterial groups that reflect common gene pools as a result of biased rates of gene transfer
