Noncontiguous operon is a genetic organization for coordinating bacterial gene expression

S. Sáenz-Lahoya, N. Bitarte, B. García, S. Burgui, M. Vergara-Irigaray, J. Valle, C. Solano, A. Toledo-Arana, and I. Lasa
PNAS January 29, 2019 116 (5) 1733-1738; published ahead of print January 29, 2019 https://doi.org/10.1073/pnas.1812746116

  1. Edited by Richard P. Novick, New York University School of Medicine, New York, NY, and approved December 11, 2018 (received for review July 26, 2018)

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Significance

In bacteria, functionally related genes are often cotranscribed in a single mRNA molecule under the same upstream promoter, forming a polycistronic operon unit. With this strategy, bacteria guarantee that production of all proteins related to a specific cellular process is simultaneously switched on or off. Here, we report the identification of a transcriptional organization consisting in operons that contain a gene(s) that is transcribed in the opposite direction to the rest of the genes of the operon. As a consequence, the resulting mRNA is fully complementary to the operon transcript. This genetic arrangement leads to mutual regulation of the overlapping transcripts expression and, thus, provides an additional strategy for coordinating the expression of functionally related genes within an operon.

Abstract

Bacterial genes are typically grouped into operons defined as clusters of adjacent genes encoding for proteins that fill related roles and are transcribed into a single polycistronic mRNA molecule. This simple organization provides an efficient mechanism to coordinate the expression of neighboring genes and is at the basis of gene regulation in bacteria. Here, we report the existence of a higher level of organization in operon structure that we named noncontiguous operon and consists in an operon containing a gene(s) that is transcribed in the opposite direction to the rest of the operon. This transcriptional architecture is exemplified by the genes menE-menC-MW1733-ytkD-MW1731 involved in menaquinone synthesis in the major human pathogen Staphylococcus aureus. We show that menE-menC-ytkD-MW1731 genes are transcribed as a single transcription unit, whereas the MW1733 gene, located between menC and ytkD, is transcribed in the opposite direction. This genomic organization generates overlapping transcripts whose expression is mutually regulated by transcriptional interference and RNase III processing at the overlapping region. In light of our results, the canonical view of operon structure should be revisited by including this operon arrangement in which cotranscription and overlapping transcription are combined to coordinate functionally related gene expression.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: ilasa{at}unavarra.es.

  • Author contributions: A.T.-A. and I.L. conceived the idea; I.L. designed research; S.S.-L., N.B., B.G., S.B., and M.V.-I. performed research; J.V., C.S., A.T.-A., and I.L. analyzed data; and I.L. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1812746116/-/DCSupplemental.

Published under the PNAS license.

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Noncontiguous operon is a genetic organization for coordinating bacterial gene expression
S. Sáenz-Lahoya, N. Bitarte, B. García, S. Burgui, M. Vergara-Irigaray, J. Valle, C. Solano, A. Toledo-Arana, I. Lasa
Proceedings of the National Academy of Sciences Jan 2019, 116 (5) 1733-1738; DOI: 10.1073/pnas.1812746116
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