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Journal of Bacteriology, April 2008, p. 2458-2469, Vol. 190, No. 7
0021-9193/08/$08.00+0     doi:10.1128/JB.01366-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Functional Overlap but Lack of Complete Cross-Complementation of Streptococcus mutans and Escherichia coli YidC Orthologs

Yuxia Dong,^2, Sara R. Palmer,^1, Adnan Hasona,¹ Shushi Nagamori,³ H. Ronald Kaback,³ Ross E. Dalbey,^2* and L. Jeannine Brady^1*

Department of Oral Biology, University of Florida, P.O. Box 100424, Gainesville, Florida 32610,¹ Department of Chemistry, The Ohio State University, Columbus, Ohio 43210,² Department of Physiology, Department of Microbiology, Immunology and Medical Genetics, Molecular Biology Institute, University of California, Los Angeles, California 90095³

Received 21 August 2007/ Accepted 23 December 2007

Oxa/YidC/Alb family proteins are chaperones involved in membrane protein insertion and assembly. Streptococcus mutans has two YidC paralogs. Elimination of yidC2, but not yidC1, results in stress sensitivity with decreased membrane-associated F₁F_o ATPase activity and an inability to initiate growth at low pH or high salt concentrations (A. Hasona, P. J. Crowley, C. M. Levesque, R. W. Mair, D. G. Cvitkovitch, A. S. Bleiweis, and L. J. Brady, Proc. Natl. Acad. Sci. USA 102:17466-17471, 2005). We now show that Escherichia coli YidC complements for acid tolerance, and partially for salt tolerance, in S. mutans lacking yidC2 and that S. mutans YidC1 or YidC2 complements growth in liquid medium, restores the proton motive force, and functions to assemble the F₁F_o ATPase in a previously engineered E. coli YidC depletion strain (J. C. Samuelson, M. Chen, F. Jiang, I. Moller, M. Wiedmann, A. Kuhn, G. J. Phillips, and R. E. Dalbey, Nature 406:637-641, 2000). Both YidC1 and YidC2 also promote membrane insertion of known YidC substrates in E. coli; however, complete membrane integrity is not fully replicated, as evidenced by induction of phage shock protein A. While both function to rescue E. coli growth in broth, a different result is observed on agar plates: growth of the YidC depletion strain is largely restored by 247YidC2, a hybrid S. mutans YidC2 fused to the YidC targeting region, but not by a similar chimera, 247YidC1, nor by YidC1 or YidC2. Simultaneous expression of YidC1 and YidC2 improves complementation on plates. This study demonstrates functional redundancy between YidC orthologs in gram-negative and gram-positive organisms but also highlights differences in their activity depending on growth conditions and species background, suggesting that the complete functional spectrum of each is optimized for the specific bacteria and environment in which they reside.

Published ahead of print on 4 January 2008.

Y.D. and S.R.P. contributed equally to this work.