On the Evolution of Chromosomal Regions with High Gene Strand Bias in Bacteria

Abstract

On circular bacterial chromosomes, the majority of genes are coded on the leading strand. This gene strand bias (GSB) ranges from up to 85% in some Bacillota to little more than 50% in other phyla. The factors defining the extent of the GSB remain to be found. Here, we report that species in the phylum Gemmatimonadota share a unique chromosome architecture, distinct from neighboring phyla: In a conserved 600 kb region around the terminus of replication, almost all genes were located on the leading strands while on the remaining part of the chromosome the strand preference was more balanced. The high strand bias (HSB) region harbors the rRNA clusters, core, and highly expressed genes. Selective pressure for reduction of collisions with DNA replication to minimize detrimental mutations can explain the conservation of essential genes in this region. Repetitive and mobile elements are underrepresented, suggesting reduced recombination frequency by structural isolation from other parts of the chromosome. We propose that the HSB region forms a distinct chromosomal domain. Gemmatimonadota chromosomes evolved mainly by expansion through horizontal gene transfer and duplications outside of the ancient HSB region. In support of our hypothesis, we could further identify two Spiroplasma strains on a similar evolutionary path.