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Heme packing motifs revealed by the crystal structure of the tetra-heme cytochrome c554 from Nitrosomonas europaea

Nature Structural Biology volume 5, pages 1005–1012 (1998)Cite this article

Abstract

Cytochrome c554 (cyt c554), a tetra-heme cytochrome from Nitrosomonas europaea, is an essential component in the biological nitrification pathway. In N. europaea, ammonia is converted to hydroxylamine, which is then oxidized to nitrite by hydroxylamine oxidoreductase (HAO). Cyt c554 functions in the latter process by accepting pairs of electrons from HAO and transferring them to a cytochrome acceptor. The crystal structure of cyt c554 at 2.6 Å resolution shows a predominantly α-helical protein with four covalently attached hemes. The four hemes are arranged in two pairs such that the planes of the porphyrin rings are almost parallel and overlapping at the edge; corresponding heme arrangements are observed in other multi-heme proteins. Striking structural similarities are evident between the tetra-heme core of cyt c554 and hemes 3–6 of HAO, which suggests an evolutionary relationship between these redox partners.

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Figure 1: The oxidation of NH3 to NO2– by Nitrosomonas europaea.
Figure 2: a.A schematic drawing illustrating the overall fold of cyt c554.
Figure 3: Heme configuration and superposition of heme stacking motifs.
Figure 4: Unusual aspects of the structure of cyt c554.
Figure 5: a, Stereoview of the GRASP35 electrostatic surface potential representation of cyt c554 illustrating the large positive ridge (right side) proposed to represent the HAO docking site.

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Acknowledgements

We thank J. Hu, L. Joshua-Tor, M. Stowell, D. Cascio, M. Soltis, H. Schindelin, C. Kisker and C. Kielkopf for experimental assistance; C. Drennan and H. Axelrod for critical reading and helpful discussions; K. Matthews and B. Crane for the microspectrophotometery; M. Carrondo for the split Soret cytochrome coordinates; and R. Timkovich for the cytochrome c552 coordinates. This work was supported by an NSF grant to A.B.H and an NIH grant to D.C.R. T.M.I. is supported by an NIH fellowship. The rotation camera facility at SSRL is supported by the NIH and Department of Energy.

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  1. Michael S.P. Logan

    Present address: Biotechnology Center for Agriculture and the Environment, Rutgers University, New Brunswick, New Jersey, 08903, USA

Authors and Affiliations

  1. Graduate Option in Biochemistry, 147-75 CH, California Institute of Technology, Pasadena, 91125, California, USA

    Tina M. Iverson

  2. Department of Biochemistry, University of Minnesota, St. Paul, 55108, Minnesota, USA

    David M. Arciero, Michael S.P. Logan & Alan B. Hooper

  3. Division of Chemistry and Chemical Engineering, 147-75 CH, California Institute of Technology, Pasadena, 91125, California, USA

    Barbara T. Hsu & Douglas C. Rees

  4. Howard Hughes Medical Institute, Pasadena , 91125, California, USA

    Douglas C. Rees

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Correspondence to Douglas C. Rees.

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Iverson, T., Arciero, D., Hsu, B. et al. Heme packing motifs revealed by the crystal structure of the tetra-heme cytochrome c554 from Nitrosomonas europaea. Nat Struct Mol Biol 5, 1005–1012 (1998). https://doi.org/10.1038/2975

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