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Operon Concatenation Is an Ancient Feature That Restricts the Potential to Rearrange Bacterial Chromosomes
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala Univ, Biomed Ctr, Dept Med Biochem & Microbiol, Uppsala, Sweden.
2019 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 36, no 9, p. 1990-2000Article in journal (Refereed) Published
Abstract [en]

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.

Place, publisher, year, edition, pages
2019. Vol. 36, no 9, p. 1990-2000
Keywords [en]
tufA, tufB, inversion, promoter-terminator overlap
National Category
Microbiology in the medical area
Identifiers
URN: urn:nbn:se:uu:diva-397120DOI: 10.1093/molbev/msz129ISI: 000493043800012PubMedID: 31132113OAI: oai:DiVA.org:uu-397120DiVA, id: diva2:1373259
Funder
Swedish Research Council, 2016-04449Swedish Research Council, 2017-03953Carl Tryggers foundation , CTS16:194Carl Tryggers foundation , CTS17:204Available from: 2019-11-26 Created: 2019-11-26 Last updated: 2019-11-26Bibliographically approved

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