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The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets

BACKGROUND: The Ferric uptake regulator (Fur) is a transcriptional regulator that controls iron homeostasis in bacteria. Although the regulatory role of Fur in Escherichia coli is well characterized, most of the studies were conducted under routine culture conditions, i.e., in ambient oxygen concent...

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Autores principales: Troxell, Bryan, Fink, Ryan C, Porwollik, Steffen, McClelland, Michael, Hassan, Hosni M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3212961/
https://www.ncbi.nlm.nih.gov/pubmed/22017966
http://dx.doi.org/10.1186/1471-2180-11-236
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author Troxell, Bryan
Fink, Ryan C
Porwollik, Steffen
McClelland, Michael
Hassan, Hosni M
author_facet Troxell, Bryan
Fink, Ryan C
Porwollik, Steffen
McClelland, Michael
Hassan, Hosni M
author_sort Troxell, Bryan
collection PubMed
description BACKGROUND: The Ferric uptake regulator (Fur) is a transcriptional regulator that controls iron homeostasis in bacteria. Although the regulatory role of Fur in Escherichia coli is well characterized, most of the studies were conducted under routine culture conditions, i.e., in ambient oxygen concentration. To reveal potentially novel aspects of the Fur regulon in Salmonella enterica serovar Typhimurium under oxygen conditions similar to that encountered in the host, we compared the transcriptional profiles of the virulent wild-type strain (ATCC 14028s) and its isogenic Δfur strain under anaerobic conditions. RESULTS: Microarray analysis of anaerobically grown Δfur S. Typhimurium identified 298 differentially expressed genes. Expression of several genes controlled by Fnr and NsrR appeared to be also dependent on Fur. Furthermore, Fur was required for the activity of the cytoplasmic superoxide disumutases (MnSOD and FeSOD). The regulation of FeSOD gene, sodB, occurred via small RNAs (i.e., the ryhB homologs, rfrA and rfrB) with the aid of the RNA chaperone Hfq. The transcription of sodA was increased in Δfur; however, the enzyme was inactive due to the incorporation of iron instead of manganese in SodA. Additionally, in Δfur, the expression of the gene coding for the ferritin-like protein (ftnB) was down-regulated, while the transcription of the gene coding for the nitric oxide (NO(·)) detoxifying flavohemoglobin (hmpA) was up-regulated. The promoters of ftnB and hmpA do not contain recognized Fur binding motifs, which indicated their probable indirect regulation by Fur. However, Fur activation of ftnB was independent of Fnr. In addition, the expression of the gene coding for the histone-like protein, H-NS (hns) was increased in Δfur. This may explain the observed down-regulation of the tdc operon, responsible for the anaerobic degradation of threonine, and ftnB in Δfur. CONCLUSIONS: This study determined that Fur is a positive factor in ftnB regulation, while serving to repress the expression of hmpA. Furthermore, Fur is required for the proper expression and activation of the antioxidant enzymes, FeSOD and MnSOD. Finally, this work identified twenty-six new targets of Fur regulation, and demonstrates that H-NS repressed genes are down-regulated in Δfur.
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spelling pubmed-32129612011-11-11 The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets Troxell, Bryan Fink, Ryan C Porwollik, Steffen McClelland, Michael Hassan, Hosni M BMC Microbiol Research Article BACKGROUND: The Ferric uptake regulator (Fur) is a transcriptional regulator that controls iron homeostasis in bacteria. Although the regulatory role of Fur in Escherichia coli is well characterized, most of the studies were conducted under routine culture conditions, i.e., in ambient oxygen concentration. To reveal potentially novel aspects of the Fur regulon in Salmonella enterica serovar Typhimurium under oxygen conditions similar to that encountered in the host, we compared the transcriptional profiles of the virulent wild-type strain (ATCC 14028s) and its isogenic Δfur strain under anaerobic conditions. RESULTS: Microarray analysis of anaerobically grown Δfur S. Typhimurium identified 298 differentially expressed genes. Expression of several genes controlled by Fnr and NsrR appeared to be also dependent on Fur. Furthermore, Fur was required for the activity of the cytoplasmic superoxide disumutases (MnSOD and FeSOD). The regulation of FeSOD gene, sodB, occurred via small RNAs (i.e., the ryhB homologs, rfrA and rfrB) with the aid of the RNA chaperone Hfq. The transcription of sodA was increased in Δfur; however, the enzyme was inactive due to the incorporation of iron instead of manganese in SodA. Additionally, in Δfur, the expression of the gene coding for the ferritin-like protein (ftnB) was down-regulated, while the transcription of the gene coding for the nitric oxide (NO(·)) detoxifying flavohemoglobin (hmpA) was up-regulated. The promoters of ftnB and hmpA do not contain recognized Fur binding motifs, which indicated their probable indirect regulation by Fur. However, Fur activation of ftnB was independent of Fnr. In addition, the expression of the gene coding for the histone-like protein, H-NS (hns) was increased in Δfur. This may explain the observed down-regulation of the tdc operon, responsible for the anaerobic degradation of threonine, and ftnB in Δfur. CONCLUSIONS: This study determined that Fur is a positive factor in ftnB regulation, while serving to repress the expression of hmpA. Furthermore, Fur is required for the proper expression and activation of the antioxidant enzymes, FeSOD and MnSOD. Finally, this work identified twenty-six new targets of Fur regulation, and demonstrates that H-NS repressed genes are down-regulated in Δfur. BioMed Central 2011-10-21 /pmc/articles/PMC3212961/ /pubmed/22017966 http://dx.doi.org/10.1186/1471-2180-11-236 Text en Copyright ©2011 Troxell et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Troxell, Bryan
Fink, Ryan C
Porwollik, Steffen
McClelland, Michael
Hassan, Hosni M
The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets
title The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets
title_full The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets
title_fullStr The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets
title_full_unstemmed The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets
title_short The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets
title_sort fur regulon in anaerobically grown salmonella enterica sv. typhimurium: identification of new fur targets
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3212961/
https://www.ncbi.nlm.nih.gov/pubmed/22017966
http://dx.doi.org/10.1186/1471-2180-11-236
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