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Journal of Bacteriology, January 2009, p. 42-51, Vol. 191, No. 1
0021-9193/09/$08.00+0     doi:10.1128/JB.01208-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

A Novel Class of Modular Transporters for Vitamins in Prokaryotes {triangledown} ,{dagger}

Dmitry A. Rodionov,1,2* Peter Hebbeln,3 Aymerick Eudes,4 Josy ter Beek,5 Irina A. Rodionova,1 Guus B. Erkens,5 Dirk J. Slotboom,5 Mikhail S. Gelfand,2,6 Andrei L. Osterman,1 Andrew D. Hanson,4 and Thomas Eitinger3*

Burnham Institute for Medical Research, La Jolla, California 92037,1 Institute for Information Transmission Problems, the A. A. Kharkevich Institute, RAS, Bolshoi Karetny pereulok 19, Moscow 127994, Russia,2 Institut für Biologie/Mikrobiologie, Humboldt Universität zu Berlin, Chausseestraße 117, 10115 Berlin, Germany,3 Horticultural Sciences Department, University of Florida, Gainesville, Florida 32611,4 Department of Biochemistry, University of Groningen, Groningen Biomolecular Science and Biotechnology Institute, Nijenborgh 4, 9747 AG Groningen, The Netherlands,5 Faculty of Bioengineering and Bioinformatics, Moscow State University, Vorobievy Gory 1-73, Moscow 119992, Russia6

Received 28 August 2008/ Accepted 12 October 2008

The specific and tightly controlled transport of numerous nutrients and metabolites across cellular membranes is crucial to all forms of life. However, many of the transporter proteins involved have yet to be identified, including the vitamin transporters in various human pathogens, whose growth depends strictly on vitamin uptake. Comparative analysis of the ever-growing collection of microbial genomes coupled with experimental validation enables the discovery of such transporters. Here, we used this approach to discover an abundant class of vitamin transporters in prokaryotes with an unprecedented architecture. These transporters have energy-coupling modules comprised of a conserved transmembrane protein and two nucleotide binding proteins similar to those of ATP binding cassette (ABC) transporters, but unlike ABC transporters, they use small integral membrane proteins to capture specific substrates. We identified 21 families of these substrate capture proteins, each with a different specificity predicted by genome context analyses. Roughly half of the substrate capture proteins (335 cases) have a dedicated energizing module, but in 459 cases distributed among almost 100 gram-positive bacteria, including numerous human pathogens, different and unrelated substrate capture proteins share the same energy-coupling module. The shared use of energy-coupling modules was experimentally confirmed for folate, thiamine, and riboflavin transporters. We propose the name energy-coupling factor transporters for the new class of membrane transporters.

* Corresponding author. Mailing address for Dmitry A. Rodionov: Burnham Institute for Medical Research, 10901 North Torrey Pines Road, La Jolla, CA 92037. Phone: (858) 646-3100. Fax: (858) 795-5249. E-mail: rodionov{at}burnham.org. Mailing address for Thomas Eitinger: Institut für Biologie/Mikrobiologie, Humboldt Universität zu Berlin, Chausseestraße 117, 10115 Berlin, Germany. Phone: 49-30-20938103. Fax: 49-30-484982923. E-mail: thomas.eitinger{at}cms.hu-berlin.de

{triangledown} Published ahead of print on 17 October 2008.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, January 2009, p. 42-51, Vol. 191, No. 1
0021-9193/09/$08.00+0     doi:10.1128/JB.01208-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.



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