The primary and three-dimensional structures of a nine-haem cytochrome c from Desulfovibrio desulfuricans ATCC 27774 reveal a new member of the Hmc family

Pedro M. Matias, Ricardo Coelho, Inês A.C. Pereira, Ana V. Coelho, Andrew W. Thompson, Larry C. Sieker, Jean Le Gall, Maria Arménia Carrondo

Research output: Contribution to journalArticle

60 Citations (Scopus)

Abstract

Background: Haem-containing proteins are directly involved in electron transfer as well as in enzymatic functions. The nine-haem cytochrome c (9Hcc), previously described as having 12 haem groups, was isolated from cells of Desulfovibrio desulfuricans ATCC 27774, grown under both nitrate- and sulphate-respiring conditions. Results: Models for the primary and three- dimensional structures of this cytochrome, containing 292 amino acid residues and nine haem groups, were derived using the multiple wavelength anomalous dispersion phasing method and refined using 1.8 Å diffraction data to an R value of 17.0%. The nine haem groups are arranged into two tetrahaem clusters, with Fe-Fe distances and local protein fold similar to tetrahaem cytochromes c3, while the extra haem is located asymmetrically between the two clusters. Conclusions: This is the first known three-dimensional structure in which multiple copies of a tetrahaem cytochrome c3-like fold are present in the same polypeptide chain. Sequence homology was found between this cytochrome and the C-terminal region (residues 229-514) of the high molecular weight cytochrome c from Desulfovibrio vulgaris Hildenborough (DvH Hmc). A new haem arrangement in domains Ill and IV of DvH Hmc is proposed. Kinetic experiments showed that 9Hcc can be reduced by the [NiFe] hydrogenase from D. desulfuricans ATCC 27774, but that this reduction is faster in the presence of tetrahaem cytochrome c3. As Hmc has never been found in D. desulfuricans ATCC 27774, we propose that 9Hcc replaces it in this organism and is therefore probably involved in electron transfer across the membrane.

Original languageEnglish
Pages (from-to)119-130
Number of pages12
JournalStructure
Volume7
Issue number2
DOIs
Publication statusPublished - 15 Feb 1999

Keywords

  • Electron transfer
  • Hydrogen metabolism
  • MAD phasing method
  • Multihaem cytochrome c
  • Sulphate-reducing bacteria
  • Three-dimensional structure

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