Multiple regulators of the Flavohaemoglobin ( hmp ) gene of Salmonella enterica serovar Typhimurium include RamA, a tran
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O RI G I NAL PAPE R
Multiple regulators of the Flavohaemoglobin (hmp) gene of Salmonella enterica serovar Typhimurium include RamA, a transcriptional regulator conferring the multidrug resistance phenotype Elizabeth Hernández-Urzúa · David S. Zamorano-Sánchez · José Ponce-Coria · Enrique Morett · Susan Grogan · Robert K. Poole · Jorge Membrillo-Hernández Received: 4 May 2006 / Revised: 20 July 2006 / Accepted: 30 August 2006 / Published online: 6 October 2006 © Springer-Verlag 2006
Abstract Microbial Xavohaemoglobins are proteins with homology to haemoglobins from higher organisms, but clearly linked to nitric oxide (NO) metabolism by bacteria and yeast. hmp mutant strains of several bacteria are hypersensitive to NO and related compounds and hmp genes are up-regulated by the presence of NO. The regulatory mechanisms involved in hmp induction by NO and the superoxide-generating agent, methyl viologen (paraquat; PQ), are complex, but progressively being resolved. Here we show for the Wrst time that, in Salmonella enterica serovar Typhimurium, hmp transcription is increased on exposure to PQ and demonstrate that RamA, a homologue
E. Hernández-Urzúa · D. S. Zamorano-Sánchez · J. Ponce-Coria · J. Membrillo-Hernández (&) Laboratorio de Microbiología y Genética Molecular, Departamento de Biología Molecular y Biotecnología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, P.O. Box 70-228, Coyoacán, Mexico City 04510, Mexico e-mail: [email protected] S. Grogan · R. K. Poole Krebs Institute for Biomolecular Research, Department of Molecular Biology and Biotechnology, University of SheYeld, SheYeld, UK E. Morett Departamento de Ingeniería Celular y Biocatálisis, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Mexico City, Mexico Present Address: S. Grogan Department of Medicine, Section of Infectious Disease, Boston University School of Medicine, 650 Albany Street, EBRC, Room 630, Boston, MA 02118, USA
of MarA is responsible for most of the hmp paraquat regulation. In addition we demonstrate NO-dependent elevation of Salmonella hmp transcription and Hmp accumulation. In both Escherichia coli and Salmonella modest transcriptional repression of hmp is exerted by the iron responsive transcriptional repressor Fur. Finally, in contrast to previous reports, we show that in E. coli and Salmonella, hmp induction by both paraquat and sodium nitroprusside is further elevated in a fur mutant background, indicating that additional regulators are implicated in this control process. Keywords Flavohaemoglobin · Nitric oxide · Paraquat · Fur · Iron regulation · RamA
Introduction Haemoglobins are deWned as haem proteins that bind oxygen reversibly. Microbial haemoglobins can be classiWed into two broad groups. The Wrst comprises globins resembling classical myoglobin or haemoglobin as in the case of Vitreoscilla Vgb (Wakabayashi et al. 1986), or Campylobacter jejuni Cgb (Elvers et al. 2004). The second broad group comprises the chimeric Xavohaemoproteins, composed of a single poly
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