High-resolution crystal structures of two polymorphs of cytochrome c' from the purple phototrophic bacterium Rhodobacter capsulatus

Tahir H. Tahirov, Shintaro Misaki, Terry E. Meyer, Michael A. Cusanovich, Yoshiki Higuchi, Noritake Yasuoka

Research output: Contribution to journalArticle

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Abstract

The structures of two polymorphs of cytochrome c' from Rhodobacter capsulatus (RCCP) strain M110 have been determined by the molecular replacement method. Iron anomalous scattering data were used to confirm the molecular replacement solution. The structures were refined at 1.72 Å and 2.0 Å resolution to R-values of 15.0% and 16.3%, respectively The RCCP molecule is a dimer and each of the identical 129 residue subunits folds as a four-helical bundle with a covalently bound heme group in the center. This structural motif resembles that of cytochromes c' reported from Rhodospirillum molischianum (RMCP), Rhodospirillum rubrum (RRCP), Chromatium vinosum (CVCP), Achromobacter xyloseoxidans (AXCP) and Alcaligenes denitrificans (ADCP). However, the architecture of the RCCP dimer, that is, the mode of association of subunits, differs substantially from that of the other cytochromes c'. In the RCCP dimer, the subunits are roughly parallel with each other and only helix B of each subunit participates in formation of the dimer interface. Measurement of the solvent-accessible surface area indicates that the dimer interface is smaller in RCCP than in the other cytochromes c'. In RMCP, CVCP, RRCP, AXCP and ADCP the subunits cross each other to form an X shape, and two helices, A and B, of each subunit interact across the dimer interface. These results are consistent with hydrodynamic measurements, which show that there is an equilibrium between monomers and dimer in RCCP, whereas the dimer is the predominant form in the other cytochromes c' for which structures have been determined. Structural comparison of the six cytochromes c' reveal that they can be divided into two groups. In group 1 cytochromes c', CVCP and RCCP, the amino acid sequences and the folding of subunits are arranged in such a way as to allow the formation of a deep channel between helices B and C with direct solvent accessibility to the heme sixth ligand position. There is no such channel in group 2 cytochromes c', RMCP, RRCP, AXCP and ADCP. This may account, in part, for the differences in carbon monoxide binding.

Original languageEnglish (US)
Pages (from-to)467-479
Number of pages13
JournalJournal of Molecular Biology
Volume259
Issue number3
DOIs
StatePublished - Jun 14 1996

Fingerprint

Cytochromes c'
Rhodobacter capsulatus
Proteobacteria
Heme
Rhodospirillum
Achromobacter
Chromatium
Rhodospirillum rubrum
Alcaligenes
Hydrodynamics
Carbon Monoxide
Amino Acid Sequence
Iron
Ligands

Keywords

  • Cytochrome c'
  • Electron transfer protein
  • Protein structure
  • Rhodobacter capsulatus
  • X-ray crystallography

ASJC Scopus subject areas

  • Structural Biology
  • Molecular Biology

Cite this

High-resolution crystal structures of two polymorphs of cytochrome c' from the purple phototrophic bacterium Rhodobacter capsulatus. / Tahirov, Tahir H.; Misaki, Shintaro; Meyer, Terry E.; Cusanovich, Michael A.; Higuchi, Yoshiki; Yasuoka, Noritake.

In: Journal of Molecular Biology, Vol. 259, No. 3, 14.06.1996, p. 467-479.

Research output: Contribution to journalArticle

Tahirov, Tahir H. ; Misaki, Shintaro ; Meyer, Terry E. ; Cusanovich, Michael A. ; Higuchi, Yoshiki ; Yasuoka, Noritake. / High-resolution crystal structures of two polymorphs of cytochrome c' from the purple phototrophic bacterium Rhodobacter capsulatus. In: Journal of Molecular Biology. 1996 ; Vol. 259, No. 3. pp. 467-479.
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T1 - High-resolution crystal structures of two polymorphs of cytochrome c' from the purple phototrophic bacterium Rhodobacter capsulatus

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AU - Cusanovich, Michael A.

AU - Higuchi, Yoshiki

AU - Yasuoka, Noritake

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N2 - The structures of two polymorphs of cytochrome c' from Rhodobacter capsulatus (RCCP) strain M110 have been determined by the molecular replacement method. Iron anomalous scattering data were used to confirm the molecular replacement solution. The structures were refined at 1.72 Å and 2.0 Å resolution to R-values of 15.0% and 16.3%, respectively The RCCP molecule is a dimer and each of the identical 129 residue subunits folds as a four-helical bundle with a covalently bound heme group in the center. This structural motif resembles that of cytochromes c' reported from Rhodospirillum molischianum (RMCP), Rhodospirillum rubrum (RRCP), Chromatium vinosum (CVCP), Achromobacter xyloseoxidans (AXCP) and Alcaligenes denitrificans (ADCP). However, the architecture of the RCCP dimer, that is, the mode of association of subunits, differs substantially from that of the other cytochromes c'. In the RCCP dimer, the subunits are roughly parallel with each other and only helix B of each subunit participates in formation of the dimer interface. Measurement of the solvent-accessible surface area indicates that the dimer interface is smaller in RCCP than in the other cytochromes c'. In RMCP, CVCP, RRCP, AXCP and ADCP the subunits cross each other to form an X shape, and two helices, A and B, of each subunit interact across the dimer interface. These results are consistent with hydrodynamic measurements, which show that there is an equilibrium between monomers and dimer in RCCP, whereas the dimer is the predominant form in the other cytochromes c' for which structures have been determined. Structural comparison of the six cytochromes c' reveal that they can be divided into two groups. In group 1 cytochromes c', CVCP and RCCP, the amino acid sequences and the folding of subunits are arranged in such a way as to allow the formation of a deep channel between helices B and C with direct solvent accessibility to the heme sixth ligand position. There is no such channel in group 2 cytochromes c', RMCP, RRCP, AXCP and ADCP. This may account, in part, for the differences in carbon monoxide binding.

AB - The structures of two polymorphs of cytochrome c' from Rhodobacter capsulatus (RCCP) strain M110 have been determined by the molecular replacement method. Iron anomalous scattering data were used to confirm the molecular replacement solution. The structures were refined at 1.72 Å and 2.0 Å resolution to R-values of 15.0% and 16.3%, respectively The RCCP molecule is a dimer and each of the identical 129 residue subunits folds as a four-helical bundle with a covalently bound heme group in the center. This structural motif resembles that of cytochromes c' reported from Rhodospirillum molischianum (RMCP), Rhodospirillum rubrum (RRCP), Chromatium vinosum (CVCP), Achromobacter xyloseoxidans (AXCP) and Alcaligenes denitrificans (ADCP). However, the architecture of the RCCP dimer, that is, the mode of association of subunits, differs substantially from that of the other cytochromes c'. In the RCCP dimer, the subunits are roughly parallel with each other and only helix B of each subunit participates in formation of the dimer interface. Measurement of the solvent-accessible surface area indicates that the dimer interface is smaller in RCCP than in the other cytochromes c'. In RMCP, CVCP, RRCP, AXCP and ADCP the subunits cross each other to form an X shape, and two helices, A and B, of each subunit interact across the dimer interface. These results are consistent with hydrodynamic measurements, which show that there is an equilibrium between monomers and dimer in RCCP, whereas the dimer is the predominant form in the other cytochromes c' for which structures have been determined. Structural comparison of the six cytochromes c' reveal that they can be divided into two groups. In group 1 cytochromes c', CVCP and RCCP, the amino acid sequences and the folding of subunits are arranged in such a way as to allow the formation of a deep channel between helices B and C with direct solvent accessibility to the heme sixth ligand position. There is no such channel in group 2 cytochromes c', RMCP, RRCP, AXCP and ADCP. This may account, in part, for the differences in carbon monoxide binding.

KW - Cytochrome c'

KW - Electron transfer protein

KW - Protein structure

KW - Rhodobacter capsulatus

KW - X-ray crystallography

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