mRNA dynamics and alternative conformations adopted under low and high arginine concentrations control polyamine biosynthesis in Salmonella

Tamar Ben-Zvi, Alina Pushkarev, Hemda Seri, Maya Elgrably-Weiss, Kai Papenfort, Shoshy Altuvia*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

13 Scopus citations

Abstract

Putrescine belongs to the large group of polyamines, an essential class of metabolites that exists throughout all kingdoms of life. The Salmonella speF gene encodes an inducible ornithine decarboxylase that produces putrescine from ornithine. Putrescine can be also synthesized from arginine in a parallel metabolic pathway. Here, we show that speF expression is controlled at multiple levels through regulatory elements contained in a long leader sequence. At the heart of this regulation is a short open reading frame, orf34, which is required for speF production. Translation of orf34 interferes with Rho-dependent transcription termination and helps to unfold an inhibitory RNA structure sequestering speF ribosome-binding site. Two consecutive arginine codons in the conserved domain of orf34 provide a third level of speF regulation. Uninterrupted translation of orf34 under conditions of high arginine allows the formation of a speF mRNA structure that is degraded by RNase G, whereas ribosome pausing at the consecutive arginine codons in the absence of arginine enables the formation of an alternative structure that is resistant to RNase G. Thus, the rate of ribosome progression during translation of the upstream ORF influences the dynamics of speF mRNA folding and putrescine production. The identification of orf34 and its regulatory functions provides evidence for the evolutionary conservation of ornithine decarboxylase regulatory elements and putrescine production.

Original languageAmerican English
Article numbere1007646
JournalPLoS Genetics
Volume15
Issue number2
DOIs
StatePublished - Feb 2019

Bibliographical note

Funding Information:
S.A. acknowledges funding by the German-Israeli Foundation (G-1311-416.13/2015); the Israel Science Foundation founded by The Israel Academy of Sciences and Humanities (711/13), the Israel Centers of Research Excellence (ICORE), Chromatin and RNA (1796/12) and by Deutsch- lsraelische Projektkooperation (AM 441/1-1 SO 568/1-1). K.P acknowledges funding by the German Research Foundation (DFG – SPP2002 and Exc114-2), the Human Frontier Science Program (CDA00024/2016-C), German-Israeli Foundation (G-2411-416.13/2016), and the European Research Council (StG-758212).

Publisher Copyright:
© 2019 Ben-Zvi et al. http://creativecommons.org/licenses/by/4.0/.

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