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The Rhizobium leguminosarum regulator IrrA affects the transcription of a wide range of genes in response to Fe availability

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Abstract

We show that an unusual transcriptional regulator, called IrrA, regulates many genes in the symbiotic N2-fixing bacterium Rhizobium leguminosarum in response to iron availability. Several operons in R. leguminosarum are expressed at lower levels in cells grown in Fe-depleted compared to Fe-replete medium. These include hemA1, which encodes the haem biosynthesis enzyme amino-levulinic acid synthase; sufS2BCDS1XA, which specify enzymes for FeS cluster synthesis; rirA, a global, Fe-responsive transcriptional repressor; RL0400, which likely encodes an unusual FeS cluster scaffold; and the possible ferri-siderophore ABC transporter rrp1. Reduced expression in Fe-depleted medium was effected by IrrA, a member of the Fur super-family, which in Bradyrhizobium, the symbiont of soybeans, and in the mammalian pathogen Brucella, is unstable in Fe-replete conditions, due to an interaction with haem. The R. leguminosarum IrrA likely interacts with ICE (iron-control element) motifs, conserved sequences near the promoters of its target genes. The rirA, sufS2BCDS1XA and rrp1 genes are also known to be regulated by RirA, which represses their expression in Fe-replete medium. We present a possible model for iron-responsive gene regulation in Rhizobium, in which the IrrA and RirA regulators, working in parallel, respond to the intracellular availability of haem and, possibly, of FeS clusters respectively. Thus, these regulators may sense the physiological consequences of extraneous Fe concentrations, rather than the concentration of Fe per se, as happens in those bacteria (e.g. Escherichia coli) in which the ferric uptake regulator Fur is the global Fe-responsive gene regulator.

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Acknowledgements

Our thanks go to Nick le Brun and Jason Crack for useful discussions and to the BBSRC for funding. D.R. was supported by the Russian Fund of Basic Research (04-04-49361) and the Russian Academy of Sciences (Program “Molecular and Cellular Biology”). We are grateful to Gesine Rudolph and Hans-Martin Fischer for useful discussions.

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Author notes

  1. Dmitry A. Rodionov

    Present address: The Burnham Institute, 10901 North Torrey Pines Road, La Jolla, CA, 92037, USA

Authors and Affiliations

  1. School of Biological Sciences, University of East Anglia, NR4 7TJ, Norwich, UK

    Jonathan D. Todd & Andrew W. B. Johnston

  2. Department of Molecular Microbiology, John Innes Centre, Norwich Research Park, Colney Lane, NR4 7UH, Norwich, UK

    Gary Sawers

  3. Institute for Information Transmission Problems RAS, Bolshoi Karetny per 19, 127994, Moscow, Russia

    Dmitry A. Rodionov

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  1. Jonathan D. Todd
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  2. Gary Sawers
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  3. Dmitry A. Rodionov
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  4. Andrew W. B. Johnston
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Correspondence to Andrew W. B. Johnston.

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Todd, J.D., Sawers, G., Rodionov, D.A. et al. The Rhizobium leguminosarum regulator IrrA affects the transcription of a wide range of genes in response to Fe availability. Mol Genet Genomics 275, 564–577 (2006). https://doi.org/10.1007/s00438-006-0115-y

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