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Applied and Environmental Microbiology, July 2001, p. 3236-3244, Vol. 67, No. 7
0099-2240/01/$04.00+0   DOI: 10.1128/AEM.67.7.3236-3244.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Identification of a Small Tetraheme Cytochrome c and a Flavocytochrome c as Two of the Principal Soluble Cytochromes c in Shewanella oneidensis Strain MR1

A. I. Tsapin,1 I. Vandenberghe,2 K. H. Nealson,1,* J. H. Scott,3 T. E. Meyer,4 M. A. Cusanovich,4 E. Harada,5 T. Kaizu,5 H. Akutsu,5,6 D. Leys,2 and J. J. Van Beeumen2,*

Jet Propulsion Laboratory, California Institute of Technology, Pasadena, California 911091; Laboratory of Protein Biochemistry and Protein Engineering, Department of Biochemistry, Physiology, and Microbiology, University of Ghent, B-9000 Ghent, Belgium2; Carnegie Institution of Washington, Washington, D.C. 200153; Department of Biochemistry and Molecular Biophysics, University of Arizona, Tucson, Arizona 857214; and Yokohama National University, Hodogaya-ku, Yokohama 240-8501,5 and Institute for Protein Research, Osaka University, Suita 565-0871,6 Japan

Received 11 October 2000/Accepted 7 March 2001

Two abundant, low-redox-potential cytochromes c were purified from the facultative anaerobe Shewanella oneidensis strain MR1 grown anaerobically with fumarate. The small cytochrome was completely sequenced, and the genes coding for both proteins were cloned and sequenced. The small cytochrome c contains 91 residues and four heme binding sites. It is most similar to the cytochromes c from Shewanella frigidimarina (formerly Shewanella putrefaciens) NCIMB400 and the unclassified bacterial strain H1R (64 and 55% identity, respectively). The amount of the small tetraheme cytochrome is regulated by anaerobiosis, but not by fumarate. The larger of the two low-potential cytochromes contains tetraheme and flavin domains and is regulated by anaerobiosis and by fumarate and thus most nearly corresponds to the flavocytochrome c-fumarate reductase previously characterized from S. frigidimarina to which it is 59% identical. However, the genetic context of the cytochrome genes is not the same for the two Shewanella species, and they are not located in multicistronic operons. The small cytochrome c and the cytochrome domain of the flavocytochrome c are also homologous, showing 34% identity. Structural comparison shows that the Shewanella tetraheme cytochromes are not related to the Desulfovibrio cytochromes c3 but define a new folding motif for small multiheme cytochromes c.

* Corresponding author. Mailing address for K. H. Nealson: Jet Propulsion Laboratory, MS 183-301, 4800 Oak Grove Dr., California Institute of Technology, Pasadena, CA 91109-8099. Phone: (818) 354-9219. Fax: (818) 393-4445. E-mail: knealson{at}jpl.nasa.gov. Mailing address for J. J. Van Beeumen: Department of Biochemistry, Physiology, and Microbiology, Laboratory of Protein Biochemistry and Protein Engineering, University of Ghent, B-9000 Ghent, Belgium. Phone: 32-9-264-5109. Fax: 32-9-264-5338. E-mail: Jozef.VanBeemen{at}rug.ac.be.

Applied and Environmental Microbiology, July 2001, p. 3236-3244, Vol. 67, No. 7
0099-2240/01/$04.00+0   DOI: 10.1128/AEM.67.7.3236-3244.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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