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Open Access Highly Accessed Research article

Campylobacter jejuni dsb gene expression is regulated by iron in a Fur-dependent manner and by a translational coupling mechanism

Anna D Grabowska12, Michał P Wandel13, Anna M Łasica1, Monika Nesteruk14, Paula Roszczenko1, Agnieszka Wyszyńska1, Renata Godlewska1 and Elzbieta K Jagusztyn-Krynicka1*

Author Affiliations

1 Department of Bacterial Genetics, Institute of Microbiology, University of Warsaw, Miecznikowa 1, 02-096, Warsaw, Poland

2 Department of Molecular Mechanisms of Mycobacterial Infections, Institute of Pharmacology and Structural Biology, 205, route de Narbonne, 31077 Toulouse cedex, France

3 Division of Protein and Nucleic Acid Chemistry MRC Laboratory of Molecular Biology Hills Road, Cambridge, CB2 0QH, UK

4 Department of Gastroenterology, The Medical Centre of Postgraduate Education, Marymoncka 99/103, 01-813 Warsaw, Poland

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BMC Microbiology 2011, 11:166  doi:10.1186/1471-2180-11-166

Published: 25 July 2011

Abstract

Background

Many bacterial extracytoplasmic proteins are stabilized by intramolecular disulfide bridges that are formed post-translationally between their cysteine residues. This protein modification plays an important role in bacterial pathogenesis, and is facilitated by the Dsb (disulfide bond) family of the redox proteins. These proteins function in two parallel pathways in the periplasmic space: an oxidation pathway and an isomerization pathway. The Dsb oxidative pathway in Campylobacter jejuni is more complex than the one in the laboratory E. coli K-12 strain.

Results

In the C. jejuni 81-176 genome, the dsb genes of the oxidative pathway are arranged in three transcriptional units: dsbA2-dsbB-astA, dsbA1 and dba-dsbI. Their transcription responds to an environmental stimulus - iron availability - and is regulated in a Fur-dependent manner. Fur involvement in dsb gene regulation was proven by a reporter gene study in a C. jejuni wild type strain and its isogenic fur mutant. An electrophoretic mobility shift assay (EMSA) confirmed that analyzed genes are members of the Fur regulon but each of them is regulated by a disparate mechanism, and both the iron-free and the iron-complexed Fur are able to bind in vitro to the C. jejuni promoter regions. This study led to identification of a new iron- and Fur-regulated promoter that drives dsbA1 gene expression in an indirect way. Moreover, the present work documents that synthesis of DsbI oxidoreductase is controlled by the mechanism of translational coupling. The importance of a secondary dba-dsbI mRNA structure for dsbI mRNA translation was verified by estimating individual dsbI gene expression from its own promoter.

Conclusions

The present work shows that iron concentration is a significant factor in dsb gene transcription. These results support the concept that iron concentration - also through its influence on dsb gene expression - might control the abundance of extracytoplasmic proteins during different stages of infection. Our work further shows that synthesis of the DsbI membrane oxidoreductase is controlled by a translational coupling mechanism. The dba expression is not only essential for the translation of the downstream dsbI gene, but also Dba protein that is produced might regulate the activity and/or stability of DsbI.