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Journal of Bacteriology, March 2005, p. 1659-1667, Vol. 187, No. 5
0021-9193/05/$08.00+0     doi:10.1128/JB.187.5.1659-1667.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Genomic Analysis of Anaerobic Respiration in the Archaeon Halobacterium sp. Strain NRC-1: Dimethyl Sulfoxide and Trimethylamine N-Oxide as Terminal Electron Acceptors{dagger}

Jochen A. Müller1 and Shiladitya DasSarma1*

Center of Marine Biotechnology, University of Maryland Biotechnology Institute, Baltimore, Maryland1

Received 12 October 2004/ Accepted 6 December 2004

We have investigated anaerobic respiration of the archaeal model organism Halobacterium sp. strain NRC-1 by using phenotypic and genetic analysis, bioinformatics, and transcriptome analysis. NRC-1 was found to grow on either dimethyl sulfoxide (DMSO) or trimethylamine N-oxide (TMAO) as the sole terminal electron acceptor, with a doubling time of 1 day. An operon, dmsREABCD, encoding a putative regulatory protein, DmsR, a molybdopterin oxidoreductase of the DMSO reductase family (DmsEABC), and a molecular chaperone (DmsD) was identified by bioinformatics and confirmed as a transcriptional unit by reverse transcriptase PCR analysis. dmsR, dmsA, and dmsD in-frame deletion mutants were individually constructed. Phenotypic analysis demonstrated that dmsR, dmsA, and dmsD are required for anaerobic respiration on DMSO and TMAO. The requirement for dmsR, whose predicted product contains a DNA-binding domain similar to that of the Bat family of activators (COG3413), indicated that it functions as an activator. A cysteine-rich domain was found in the dmsR gene, which may be involved in oxygen sensing. Microarray analysis using a whole-genome 60-mer oligonucleotide array showed that the dms operon is induced during anaerobic respiration. Comparison of dmsR+ and {Delta}dmsR strains by use of microarrays showed that the induction of the dmsEABCD operon is dependent on a functional dmsR gene, consistent with its action as a transcriptional activator. Our results clearly establish the genes required for anaerobic respiration using DMSO and TMAO in an archaeon for the first time.

* Corresponding author. Mailing address: Center of Marine Biotechnology, University of Maryland Biotechnology Institute, 701 E. Pratt St., Suite 236, Baltimore, MD 21202. Phone: (410) 234-8847. Fax: (410) 234-8896. E-mail: dassarma{at}umbi.umd.edu.

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

Journal of Bacteriology, March 2005, p. 1659-1667, Vol. 187, No. 5
0021-9193/05/$08.00+0     doi:10.1128/JB.187.5.1659-1667.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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