ArticleMolecular biology and evolution2019
Operon Concatenation Is an Ancient Feature That Restricts the Potential to Rearrange Bacterial Chromosomes.
Article in Molecular biology and evolution, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 10 papers.
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10 citing papers in PubMed.
- Advances in Decoding Bacterial N-Terminal Proteoforms: Technologies, Challenges, and Functional Insights.Microorganisms · 2026Review
- Evolutionary constraints on RNA polymerase gene positioning in the genome of fast-growing bacteria.Nucleic acids research · 2026Article
- Advancing Desulfurization in the Model BiocatalystApplied and environmental microbiology · 2023Article
- Meta-omic profiling reveals ubiquity of genes encoding for the nitrogen-rich biopolymer cyanophycin in activated sludge microbiomes.Frontiers in microbiology · 2023Article
- Ribosomal Protein Cluster Organization in Asgard Archaea.Archaea (Vancouver, B.C.) · 2023Article
- Reconstructing the Evolutionary History of a Highly Conserved Operon Cluster in Gammaproteobacteria and Bacilli.Genome biology and evolution · 2021Article
- Discovery of multi-operon colinear syntenic blocks in microbial genomes.Bioinformatics (Oxford, England) · 2020Article
- The SNAP hypothesis: Chromosomal rearrangements could emerge from positive Selection during Niche Adaptation.PLoS genetics · 2020Article
- Antibiotic resistance by high-level intrinsic suppression of a frameshift mutation in an essential gene.Proceedings of the National Academy of Sciences of the United States of America · 2020Article
- Recent advances in understanding mitochondrial genome diversity.F1000Research · 2020Review
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3 authors.
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Abstract
The last common ancestor of the Gammaproteobacteria carried an important 40-kb chromosome section encoding 51 proteins of the transcriptional and translational machinery. These genes were organized into eight contiguous operons (rrnB-tufB-secE-rpoBC-str-S10-spc-alpha). Over 2 Gy of evolution, in different lineages, some of the operons became separated by multigene insertions. Surprisingly, in many Enterobacteriaceae, much of the ancient organization is conserved, indicating a strong selective force on the operons to remain colinear. Here, we show for one operon pair, tufB-secE in Salmonella, that an interruption of contiguity significantly reduces growth rate. Our data show that the tufB-secE operons are concatenated by an interoperon terminator-promoter overlap that plays a significant role regulating gene expression. Interrupting operon contiguity interferes with this regulation, reducing cellular fitness. Six operons of the ancestral chromosome section remain contiguous in Salmonella (tufB-secE-rpoBC and S10-spc-alpha) and, strikingly, each of these operon pairs is also connected by an interoperon terminator-promoter overlap. Accordingly, we propose that operon concatenation is an ancient feature that restricts the potential to rearrange bacterial chromosomes and can select for the maintenance of a colinear operon organization over billions of years.
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