SO2907, a putative TonB-dependent receptor, is involved in dissimilatory iron reduction by Shewanella oneidensis strain MR-1

Yufeng Qian, Liang Shi, Ming Tien

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Shewanella oneidensis strain MR-1 utilizes soluble and insoluble ferric ions as terminal electron acceptors during anaerobic respiration. The components of respiratory metabolism are localized in the membrane fractions which include the outer membrane and cytoplasmic membrane. Many of the biological components that interact with the various iron forms are proposed to be localized in these membrane fractions. To identify the iron-binding proteins acting either as an iron transporter or as a terminal iron reductase, we used metal-catalyzed oxidation reactions. This system catalyzed the oxidation of amino acids in close proximity to the iron binding site. The carbonyl groups formed from this oxidation can then be labeled with fluoresceinamine (FLNH 2). The peptide harboring the FLNH 2 can then be proteolytically digested, purified by HPLC and then identified by MALDI-TOF tandem MS. A predominant peptide was identified to be part of SO2907 that encodes a putative TonB-dependent receptor. Compared with wild type (wt), the so2907 gene deletion (ΔSO2907) mutant has impaired ability to reduce soluble Fe(III), but retains the same ability to respire oxygen or fumarate as the wt. The ΔSO2907 mutant was also impacted in reduction of insoluble iron. Iron binding assays using isothermal titration calorimetry and fluorescence tryptophan quenching demonstrated that a truncated form of heterologous- expressed SO2907 that contains the Fe(III) binding site, is capable of binding soluble Fe(III) forms with K d of approximate 50 μM. To the best of our knowledge, this is the first report of the physiological role of SO2907 in Fe(III) reduction by MR-1.

Original languageEnglish (US)
Pages (from-to)33973-33980
Number of pages8
JournalJournal of Biological Chemistry
Volume286
Issue number39
DOIs
StatePublished - Oct 30 2011

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Shewanella
Iron
Membranes
Oxidation
Binding Sites
Iron-Binding Proteins
Fumarates
Peptides
Calorimetry
Matrix-Assisted Laser Desorption-Ionization Mass Spectrometry
Gene Deletion
Titration
Metabolism
Tryptophan
Quenching
Assays
Respiration
Genes
Fluorescence
Metals

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Molecular Biology
  • Cell Biology

Cite this

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title = "SO2907, a putative TonB-dependent receptor, is involved in dissimilatory iron reduction by Shewanella oneidensis strain MR-1",
abstract = "Shewanella oneidensis strain MR-1 utilizes soluble and insoluble ferric ions as terminal electron acceptors during anaerobic respiration. The components of respiratory metabolism are localized in the membrane fractions which include the outer membrane and cytoplasmic membrane. Many of the biological components that interact with the various iron forms are proposed to be localized in these membrane fractions. To identify the iron-binding proteins acting either as an iron transporter or as a terminal iron reductase, we used metal-catalyzed oxidation reactions. This system catalyzed the oxidation of amino acids in close proximity to the iron binding site. The carbonyl groups formed from this oxidation can then be labeled with fluoresceinamine (FLNH 2). The peptide harboring the FLNH 2 can then be proteolytically digested, purified by HPLC and then identified by MALDI-TOF tandem MS. A predominant peptide was identified to be part of SO2907 that encodes a putative TonB-dependent receptor. Compared with wild type (wt), the so2907 gene deletion (ΔSO2907) mutant has impaired ability to reduce soluble Fe(III), but retains the same ability to respire oxygen or fumarate as the wt. The ΔSO2907 mutant was also impacted in reduction of insoluble iron. Iron binding assays using isothermal titration calorimetry and fluorescence tryptophan quenching demonstrated that a truncated form of heterologous- expressed SO2907 that contains the Fe(III) binding site, is capable of binding soluble Fe(III) forms with K d of approximate 50 μM. To the best of our knowledge, this is the first report of the physiological role of SO2907 in Fe(III) reduction by MR-1.",
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SO2907, a putative TonB-dependent receptor, is involved in dissimilatory iron reduction by Shewanella oneidensis strain MR-1. / Qian, Yufeng; Shi, Liang; Tien, Ming.

In: Journal of Biological Chemistry, Vol. 286, No. 39, 30.10.2011, p. 33973-33980.

Research output: Contribution to journalArticle

TY - JOUR

T1 - SO2907, a putative TonB-dependent receptor, is involved in dissimilatory iron reduction by Shewanella oneidensis strain MR-1

AU - Qian, Yufeng

AU - Shi, Liang

AU - Tien, Ming

PY - 2011/10/30

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N2 - Shewanella oneidensis strain MR-1 utilizes soluble and insoluble ferric ions as terminal electron acceptors during anaerobic respiration. The components of respiratory metabolism are localized in the membrane fractions which include the outer membrane and cytoplasmic membrane. Many of the biological components that interact with the various iron forms are proposed to be localized in these membrane fractions. To identify the iron-binding proteins acting either as an iron transporter or as a terminal iron reductase, we used metal-catalyzed oxidation reactions. This system catalyzed the oxidation of amino acids in close proximity to the iron binding site. The carbonyl groups formed from this oxidation can then be labeled with fluoresceinamine (FLNH 2). The peptide harboring the FLNH 2 can then be proteolytically digested, purified by HPLC and then identified by MALDI-TOF tandem MS. A predominant peptide was identified to be part of SO2907 that encodes a putative TonB-dependent receptor. Compared with wild type (wt), the so2907 gene deletion (ΔSO2907) mutant has impaired ability to reduce soluble Fe(III), but retains the same ability to respire oxygen or fumarate as the wt. The ΔSO2907 mutant was also impacted in reduction of insoluble iron. Iron binding assays using isothermal titration calorimetry and fluorescence tryptophan quenching demonstrated that a truncated form of heterologous- expressed SO2907 that contains the Fe(III) binding site, is capable of binding soluble Fe(III) forms with K d of approximate 50 μM. To the best of our knowledge, this is the first report of the physiological role of SO2907 in Fe(III) reduction by MR-1.

AB - Shewanella oneidensis strain MR-1 utilizes soluble and insoluble ferric ions as terminal electron acceptors during anaerobic respiration. The components of respiratory metabolism are localized in the membrane fractions which include the outer membrane and cytoplasmic membrane. Many of the biological components that interact with the various iron forms are proposed to be localized in these membrane fractions. To identify the iron-binding proteins acting either as an iron transporter or as a terminal iron reductase, we used metal-catalyzed oxidation reactions. This system catalyzed the oxidation of amino acids in close proximity to the iron binding site. The carbonyl groups formed from this oxidation can then be labeled with fluoresceinamine (FLNH 2). The peptide harboring the FLNH 2 can then be proteolytically digested, purified by HPLC and then identified by MALDI-TOF tandem MS. A predominant peptide was identified to be part of SO2907 that encodes a putative TonB-dependent receptor. Compared with wild type (wt), the so2907 gene deletion (ΔSO2907) mutant has impaired ability to reduce soluble Fe(III), but retains the same ability to respire oxygen or fumarate as the wt. The ΔSO2907 mutant was also impacted in reduction of insoluble iron. Iron binding assays using isothermal titration calorimetry and fluorescence tryptophan quenching demonstrated that a truncated form of heterologous- expressed SO2907 that contains the Fe(III) binding site, is capable of binding soluble Fe(III) forms with K d of approximate 50 μM. To the best of our knowledge, this is the first report of the physiological role of SO2907 in Fe(III) reduction by MR-1.

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