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Electron transfer between periplasmic formate dehydrogenase and cytochromes c in Desulfovibrio desulfuricans ATCC 27774

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Abstract

Desulfovibrio spp. are sulfate-reducing organisms characterized by having multiple periplasmic hydrogenases and formate dehydrogenases (FDHs). In contrast to enzymes in most bacteria, these enzymes do not reduce directly the quinone pool, but transfer electrons to soluble cytochromes c. Several studies have investigated electron transfer with hydrogenases, but comparatively less is known about FDHs. In this work we conducted experiments to assess potential electron transfer pathways resulting from formate oxidation in Desulfovibrio desulfuricans ATCC 27774. This organism can grow on sulfate and on nitrate, and contains a single soluble periplasmic FDH that includes a cytochrome c 3 like subunit (FdhABC3). It has also a unique cytochrome c composition, including two cytochromes c not yet isolated from other species, the split-Soret and nine-heme cytochromes, besides a tetraheme type I cytochrome c 3 (TpIc 3). The FDH activity and cytochrome composition of cells grown with lactate or formate and nitrate or sulfate were determined, and the electron transfer between FDH and these cytochromes was investigated. We studied also the reduction of the Dsr complex and of the monoheme cytochrome c-553, previously proposed to be the physiological partner of FDH. FdhABC3 was able to reduce the c-553, TpIc 3, and split-Soret cytochromes with a high rate. For comparison, the same experiments were performed with the [NiFe] hydrogenase from the same organism. This study shows that FdhABC3 can directly reduce the periplasmic cytochrome c network, feeding electrons into several alternative metabolic pathways, which explains the advantage of not having an associated membrane subunit.

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Acknowledgments

We thank Sofia S. Venceslau for providing the Dsr complex. This work was supported by research grants PTDC/QUI-BIQ/100591/2008 funded by Fundação para a Ciência e Tecnologia (FCT, MCES, Portugal) and the FEDER program. S.M.S was supported by FCT PhD fellowship SFRH/BD/24312/2005.

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Authors and Affiliations

  1. Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Av. da Republica, EAN, 2780-157, Oeiras, Portugal

    Sofia Marques da Silva, Isabel Pacheco & Inês A. Cardoso Pereira

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  1. Sofia Marques da Silva
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  2. Isabel Pacheco
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  3. Inês A. Cardoso Pereira
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Correspondence to Inês A. Cardoso Pereira.

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da Silva, S.M., Pacheco, I. & Pereira, I.A.C. Electron transfer between periplasmic formate dehydrogenase and cytochromes c in Desulfovibrio desulfuricans ATCC 27774. J Biol Inorg Chem 17, 831–838 (2012). https://doi.org/10.1007/s00775-012-0900-5

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  • DOI: https://doi.org/10.1007/s00775-012-0900-5

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