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Genome replication and cell division control by the methylation-sensitive GcrA regulator in Agrobacterium tumefaciens

ABSTRACT: Bacteria with complex genomes including secondary chromosomes and/or megaplasmids face unique challenges when controlling their cell cycle: they not only need to coordinate genome replication with other cell cycle events such as cell growth and cell division, but also to synchronize the replication of different replicons. In Alphaproteobacteria, replication and maintenance of large extrachromosomal replicons is usually dependent on RepABC modules, as seen for the plant pathogen Agrobacterium tumefaciens. In this study, we demonstrate that the conserved GcrA protein is an essential methylation-dependent transcriptional regulator playing at least two critical roles during the A. tumefaciens cell cycle. First, GcrA is required for the on-time and synchronized firing of the three RepABC-dependent origins of replication of A. tumefaciens that are needed for chromosomal and megaplasmid replication. Second, GcrA triggers the expression of several essential cell division genes for the timely and essential assembly of a functional divisome. These findings highlight how this conserved global regulator can control and then synchronize a variety of essential cell cycle events in Alphaproteobacteria with complex genomes, notably coordinating the maintenance of several RepABC-dependent replicons with cell division.

ORGANISM(S): Agrobacterium fabrum str. C58

PROVIDER: GSE330725 | GEO | 2026/05/18

REPOSITORIES: GEO

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Project description:Alphaproteobacteria stand out for their complex cell cycles, which are often regulated by the DivJ/PleC-DivK-DivL-CckA-ChpT-CtrA pathway. DivJ and PleC set up the polarity of the cell, thereby eventually leading to differential activation of the DNA-binding response regulator CtrA in the two nascent daughter cells. CtrA regulates replication and transcription of many genes, thereby ensuring that processes such as motility and cell division take place at the appropriate cell cycle stage. The cell cycle of the stalked budding alphaproteobacterium Hyphomonas neptunium culminates in an asymmetric cell division at the stalk-bud junction. Here, we investigate the role of the pathway from DivJ and PleC down to CtrA in this recently established model organism. Even though DivJ and PleC are localized to opposite poles, suggesting they are involved in polarity establishment inH. neptunium, DivJ, PleC and the other components of the upstream pathway (DivK and PleD) are not essential for cell cycle regulation. In contrast, the downstream part of the pathway starting from DivL is essential and involved in the regulation of important functions such as replication inhibition, cell division and motility, as shown by the identification of the (direct) regulon of CtrA. The overlap between the regulons of DivJ and PleC, DivK and CtrA is only partial, demonstrating that additional factors feeding into the pathway must be present in H. neptunium. Furthermore, unlike in other alphaproteobacteria, the regulation of CtrA throughout the cell cycle does not take place at the level of CtrA abundance in H. neptunium. All in all, the DivL-CckA-ChpT-CtrA pathway plays an essential role in the regulation of the complicated cell cycle ofH. neptunium, but several proteins feeding into CtrA remain undiscovered. The in-depth analysis of CtrA regulation in this stalked budding organism leads to hypotheses that might also hold in well-established model organisms such as Caulobacter crescentus.

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Genome replication and cell division control by the methylation-sensitive GcrA regulator in Agrobacterium tumefaciens

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