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Journal of Bacteriology, September 2005, p. 6300-6308, Vol. 187, No. 18
0021-9193/05/$08.00+0     doi:10.1128/JB.187.18.6300-6308.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Function of the Cytochrome bc₁-aa₃ Branch of the Respiratory Network in Mycobacteria and Network Adaptation Occurring in Response to Its Disruption

Limenako G. Matsoso,¹ Bavesh D. Kana,¹ Paul K. Crellin,² David J. Lea-Smith,² Assunta Pelosi,² David Powell,³ Stephanie S. Dawes,¹ Harvey Rubin,⁴ Ross L. Coppel,² and Valerie Mizrahi^1*

MRC/NHLS/WITS Molecular Mycobacteriology Research Unit, DST/NRF Centre of Excellence in Biomedical TB Research, School of Pathology, National Health Laboratory Service, and University of the Witwatersrand, Johannesburg, South Africa,¹ Department of Microbiology, Monash University, and ARC Centre for Structural and Functional Microbial Genomics, Monash, Australia,² Department of Computer Science and Software Engineering, Monash University, and the Victorian Bioinformatics Consortium, Monash, Australia,³ Division of Infectious Diseases, Department of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104⁴

Received 29 April 2005/ Accepted 15 June 2005

The aerobic electron transport chain in Mycobacterium smegmatis can terminate in one of three possible terminal oxidase complexes. The structure and function of the electron transport pathway leading from the menaquinol-menaquinone pool to the cytochrome bc₁ complex and terminating in the aa₃-type cytochrome c oxidase was characterized. M. smegmatis strains with mutations in the bc₁ complex and in subunit II of cyctochome c oxidase were found to be profoundly growth impaired, confirming the importance of this respiratory pathway for mycobacterial growth under aerobic conditions. Disruption of this pathway resulted in an adaptation of the respiratory network that is characterized by a marked up-regulation of cydAB, which encodes the bioenergetically less efficient and microaerobically induced cytochrome bd-type menaquinol oxidase that is required for the growth of M. smegmatis under O₂-limiting conditions. Further insights into the adaptation of this organism to rerouting of the electron flux through the branch terminating in the bd-type oxidase were revealed by expression profiling of the bc₁-deficient mutant strain using a partial-genome microarray of M. smegmatis that is enriched in essential genes. Although the expression profile was indicative of an increase in the reduced state of the respiratory chain, blockage of the bc₁-aa₃ pathway did not induce the sentinel genes of M. smegmatis that are induced by oxygen starvation and are regulated by the DosR two-component regulator.

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* Corresponding author. Mailing address: Molecular Mycobacteriology Research Unit, NHLS, P. O. Box 1038, Johannesburg 2000, South Africa. Phone: 2711 4899370. Fax: 27 11 4899001. E-mail: mizrahiv{at}pathology.wits.ac.za.

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

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Journal of Bacteriology, September 2005, p. 6300-6308, Vol. 187, No. 18
0021-9193/05/$08.00+0     doi:10.1128/JB.187.18.6300-6308.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

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