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April 14th, 2025
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IIB-UNSAM/IIBio-CONICET
microbiology
biorxiv

Evolutionary Constraints on RNA Polymerase Gene Positioning in the Genome of Fast-Growing Bacteria..

Larotonda, L. I.Open in Google Scholar•Ojeda, E.Open in Google Scholar•Bordignon, M. B.Open in Google Scholar•Fulgenzi, F. R.Open in Google Scholar•Comerci, D. J.Open in Google Scholar•Val, M.-E.Open in Google Scholar•Llorente, B. E.Open in Google Scholar•Mazel, D.Open in Google Scholar•Soler-Bistue, A.Open in Google Scholar

The influence of gene order within the chromosome on cellular homeostasis and genome evolution remains unclear. Bacterial chromosomes are structured along the replication origin (oriC)-terminus (ter) axis. The spatial organization of genes within the bacterial genome may influence cellular physiology, genome evolution, and transcriptional regulation. The catalytic core of the sole bacterial RNA polymerase (RNAP) is encoded by rpoB and rpoC within the universally conserved rplKAJL-rpoBC locus. In fast growing bacteria this locus is positioned near oriC linking genome organization to cellular physiology. Here, we tested the functional relevance of this chromosomal positioning by relocating rplKAJL-rpoBC within Vibrio cholerae genome. While viable, strains harboring rplKAJL-rpoBC far from oriC exhibited nutrient-dependent fitness defects. These effects correlated with reduced locus copy number and RNAP abundance per cell, rather than changes in RNAP subcellular distribution. The addition of a second rpIKAJL-rpoBC copy far from oriC abolished the phenotypes demonstrating that replication-associated gene dosage effects were the main mechanism behind these observations. Further uncoupling rpoB and rpoC from the rplKAJL-rpoBC locus revealed that fitness costs were specifically linked to RNAP gene relocation. Our results demonstrate that selective pressure maintains RNAP genes near oriC to optimize replication-associated dosage effects, ensuring efficient RNAP production during exponential growth. We discuss the relationship between gene order and ecological strategies linked to bacterial growth. Bacterial chromosomes display high genomic plasticity, yet gene order remains an underestimated factor shaping cellular physiology and genome evolution.

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