JBIC Journal of Biological Inorganic Chemistry

, Volume 12, Issue 7, pp 1029–1053 | Cite as

Electron paramagnetic resonance and Mössbauer spectroscopy of intact mitochondria from respiring Saccharomyces cerevisiae

  • Brandon N. Hudder
  • Jessica Garber Morales
  • Audria Stubna
  • Eckard Münck
  • Michael P. Hendrich
  • Paul A. Lindahl
Original Paper


Mitochondria from respiring cells were isolated under anaerobic conditions. Microscopic images were largely devoid of contaminants, and samples consumed O2 in an NADH-dependent manner. Protein and metal concentrations of packed mitochondria were determined, as was the percentage of external void volume. Samples were similarly packed into electron paramagnetic resonance tubes, either in the as-isolated state or after exposure to various reagents. Analyses revealed two signals originating from species that could be removed by chelation, including rhombic Fe3+ (g = 4.3) and aqueous Mn2+ ions (g = 2.00 with Mn-based hyperfine). Three S = 5/2 signals from Fe3+ hemes were observed, probably arising from cytochrome c peroxidase and the a3:Cub site of cytochrome c oxidase. Three Fe/S-based signals were observed, with averaged g values of 1.94, 1.90 and 2.01. These probably arise, respectively, from the [Fe2S2]+ cluster of succinate dehydrogenase, the [Fe2S2]+ cluster of the Rieske protein of cytochrome bc 1, and the [Fe3S4]+ cluster of aconitase, homoaconitase or succinate dehydrogenase. Also observed was a low-intensity isotropic g = 2.00 signal arising from organic-based radicals, and a broad signal with g ave = 2.02. Mössbauer spectra of intact mitochondria were dominated by signals from Fe4S4 clusters (60–85% of Fe). The major feature in as-isolated samples, and in samples treated with ethylenebis(oxyethylenenitrilo)tetraacetic acid, dithionite or O2, was a quadrupole doublet with ΔE Q = 1.15 mm/s and δ = 0.45 mm/s, assigned to [Fe4S4]2+ clusters. Substantial high-spin non-heme Fe2+ (up to 20%) and Fe3+ (up to 15%) species were observed. The distribution of Fe was qualitatively similar to that suggested by the mitochondrial proteome.


Iron Sulfur Cluster assembly Heme biosynthesis Non-heme 



Coenzyme Q




Ethylenediaminetetraacetic acid


Ethylenebis(oxyethylenenitrilo)tetraacetic acid


Electron paramagnetic resonance


Electron transfer flavoprotein


N-(2-Hydroxyethyl)piperazine-N′-ethanesulfonic acid


Inner membrane


Intermembrane space


Normal hydrogen electrode


Outer membrane

SH buffer

0.6 M sorbitol/20 mM N-(2-hydroxyethyl)piperazine-N′-ethanesulfonic acid buffer pH 7.4

SP buffer

1.2 M sorbitol/20 mM potassium phosphate buffer pH 7.4



We thank the following people: Art Johnson and Holly Cargill (Department of Biochemistry and Biophysics, Texas A&M University) for instructions on isolating mitochondria; Rola Barhoumi (Image Analysis Laboratory, Texas A&M University) and Anne Ellis (Microscopy and Imaging Center, Texas A&M University) for collecting microscopic images; Jinny Johnson (Protein Chemistry Laboratory, Texas A&M University) for performing amino acid analyses; David P. Giedroc (Department of Biochemistry and Biophysics, Texas A&M University) for access to his atomic absorption spectrophotometer; William James (Department of Chemistry, Texas A&M University) for training on and assistance with the inductively coupled plasma mass spectrometer; Shelly Henderson Possi for help in isolating some batches and in measuring O2 consumption; Tanner Freeman for preparing one of the EPR samples; and Roland Lill for helpful discussion.

This study was supported by the Robert A. Welch Foundation (A1170) and The National Institutes of Health [GM077387 (M.P.H.), EB001475 (E.M.) and The Chemistry Biology Interface training program (B.N.H. and J.G)].

Supplementary material


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Copyright information

© SBIC 2007

Authors and Affiliations

  • Brandon N. Hudder
    • 1
  • Jessica Garber Morales
    • 1
  • Audria Stubna
    • 2
  • Eckard Münck
    • 2
  • Michael P. Hendrich
    • 2
  • Paul A. Lindahl
    • 1
    • 3
  1. 1.Department of ChemistryTexas A&M UniversityCollege StationUSA
  2. 2.Department of ChemistryCarnegie Mellon UniversityPittsburghUSA
  3. 3.Department of Biochemistry and BiophysicsTexas A&M UniversityCollege StationUSA

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