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Efficient Electron Transfer in a Protein Network Lacking Specific Interactions

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Francesca Meschi†, Frank Wiertz‡, Linda Klauss‡, Anneloes Blok‡, Bernd Ludwig§, Angelo Merli†, Hendrik A. Heering‡, Gian Luigi Rossi†, and Marcellus Ubbink*‡

Department of Biochemistry and Molecular Biology, University of Parma, 43100 Parma, Italy

Institute of Chemistry, Leiden University, P.O. Box 9502, 2300 RA Leiden, The Netherlands

Institute of Biochemistry, Molecular Genetics Group, and Cluster of Excellence Macromolecular Complexes, Goethe University, D-60438 Frankfurt, Germany

J. Am. Chem. Soc., 2011, 133 (42), pp 16861–16867

DOI: 10.1021/ja205043f

Publication Date (Web): September 14, 2011

m.ubbink@chem.leidenuniv.nl

Section:

Microbial, Algal, and Fungal Biochemistry

Abstract

In many biochemical processes, proteins need to bind partners amidst a sea of other molecules. Generally, partner selection is achieved by formation of a single-orientation complex with well-defined, short-range interactions. We describe a protein network that functions effectively in a metabolic electron transfer process but lacks such specific interactions. The soil bacterium Paracoccus denitrificans oxidizes a variety of compounds by channeling electrons into the main respiratory pathway. Upon conversion of methylamine by methylamine dehydrogenase, electrons are transported to the terminal oxidase to reduce molecular oxygen. Steady-state kinetic measurements and NMR experiments demonstrate a remarkable number of possibilities for the electron transfer, involving the cupredoxin amicyanin as well as four c-type cytochromes. The observed interactions appear to be governed exclusively by the electrostatic nature of each of the proteins. It is concluded that Paracoccus provides a pool of cytochromes for efficient electron transfer via weak, ill-defined interactions, in contrast with the view that functional biochemical interactions require well-defined molecular interactions. It is proposed that the lack of requirement for specificity in these interactions might facilitate the integration of new metabolic pathways.

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