Connection Between Chromosomal Location and Function of CtrA Phosphorelay Genes in Alphaproteobacteria

Abstract

Most bacterial chromosomes are circular, with replication starting at one origin (ori) and proceeding on both replichores toward the terminus (ter). Several studies have shown that the location of genes relative to ori and ter can have profound effects on regulatory networks and physiological processes. The CtrA phosphorelay is a gene regulatory system conserved in most alphaproteobacteria. It was first discovered in Caulobacter crescentus where it controls replication and division into a stalked and a motile cell in coordination with other factors. The locations of the ctrA gene and targets of this response regulator on the chromosome affect their expression through replication-induced DNA hemi-methylation and specific positioning along a CtrA activity gradient in the dividing cell, respectively. Here we asked to what extent the location of CtrA regulatory network genes might be conserved in the alphaproteobacteria. We determined the locations of the CtrA phosphorelay and associated genes in closed genomes with unambiguously identifiable ori from members of five alphaproteobacterial orders. The location of the phosphorelay genes was the least conserved in the Rhodospirillales followed by the Sphingomonadales. In the Rhizobiales a trend toward certain chromosomal positions could be observed. Compared to the other orders, the CtrA phosphorelay genes were conserved closer to ori in the Caulobacterales. In contrast, the genes were highly conserved closer to ter in the Rhodobacterales. Our data suggest selection pressure results in differential positioning of CtrA phosphorelay and associated genes in alphaproteobacteria, particularly in the orders Rhodobacterales, Caulobacterales and Rhizobiales that is worth deeper investigation.

Shared properties of gene transfer agent and core genes revealed by comparative genomics of Alphaproteobacteria

“…The strongest conservation of GTA gene cluster localization is also found in this order, where it is biased towards ter. This is in accordance with our previous study where the Rhodobacterales ctrA gene was also found conserved near to ter and showed the lowest number of GANTC motifs in ctrA promoter regions [56]. Hemi-methylation of this motif during replication has been found to be a signal for transcriptional activation [57].…”

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

“…A current study across 773 species, covering all major bacterial taxa, found conserved positions on the chromosome, in particular a bias towards ori and ter , for almost half of the identified gene families [33]. The ori - or ter -proximal position of regulatory genes can be strongly conserved across an order but can also show distinct evolutionary trajectories between phyla [34,35]. Exceptional genome architectures, defying the general evolutionary trend within a phylum, have also been found [30,36].…”

On the evolution of chromosomal regions with high gene strand bias in bacteria

“…A current study across 773 species, covering all major bacterial taxa, found conserved positions on the chromosome, in particular a bias toward ori and ter , for almost half of the identified gene families ( 34 ). The ori - or ter -proximal position of regulatory genes can be strongly conserved across an order but can also show distinct evolutionary trajectories between phyla ( 35 , 36 ). Exceptional genome architectures, defying the general evolutionary trend within a phylum, have also been found.…”