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Journal of Bacteriology, March 2007, p. 2283-2290, Vol. 189, No. 6
0021-9193/07/$08.00+0     doi:10.1128/JB.01698-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

The cymA Gene, Encoding a Tetraheme c-Type Cytochrome, Is Required for Arsenate Respiration in Shewanella Species{triangledown}

Julie N. Murphy and Chad W. Saltikov*

Department of Environmental Toxicology, University of California, Santa Cruz, Santa Cruz, California 95064

Received 2 November 2006/ Accepted 21 December 2006

In Shewanella sp. strain ANA-3, utilization of arsenate as a terminal electron acceptor is conferred by a two-gene operon, arrAB, which lacks a gene encoding a membrane-anchoring subunit for the soluble ArrAB protein complex. Analysis of the genome sequence of Shewanella putrefaciens strain CN-32 showed that it also contained the same arrAB operon with 100% nucleotide identity. Here, we report that CN-32 respires arsenate and that this metabolism is dependent on arrA and an additional gene encoding a membrane-associated tetraheme c-type cytochrome, cymA. Deletion of cymA in ANA-3 also eliminated growth on and reduction of arsenate. The {Delta}cymA strains of CN-32 and ANA-3 negatively affected the reduction of Fe(III) and Mn(IV) but not growth on nitrate. Unlike the CN-32 {Delta}cymA strain, growth on fumarate was absent in the {Delta}cymA strain of ANA-3. Both homologous and heterologous complementation of cymA in trans restored growth on arsenate in {Delta}cymA strains of both CN-32 and ANA-3. Transcription patterns of cymA showed that it was induced under anaerobic conditions in the presence of fumarate and arsenate. Nitrate-grown cells exhibited the greatest level of cymA expression in both wild-type strains. Lastly, site-directed mutagenesis of the first Cys to Ser in each of the four CXXCH c-heme binding motifs of the CN-32 CymA nearly eliminated growth on and reduction of arsenate. Together, these results indicate that the biochemical mechanism of arsenate respiration and reduction requires the interactions of ArrAB with a membrane-associated tetraheme cytochrome, which in the non-arsenate-respiring Shewanella species Shewanella oneidensis strain MR-1, has pleiotropic effects on Fe(III), Mn(IV), dimethyl sulfoxide, nitrate, nitrite, and fumarate respiration.

* Corresponding author. Mailing address: Department of Environmental Toxicology, University of California, Santa Cruz, Santa Cruz, CA 95064. Phone: (831) 459-5520. Fax: (831) 459-3524. E-mail: saltikov{at}etox.ucsc.edu.

{triangledown} Published ahead of print on 5 January 2007.

Journal of Bacteriology, March 2007, p. 2283-2290, Vol. 189, No. 6
0021-9193/07/$08.00+0     doi:10.1128/JB.01698-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Murphy, J. N., Saltikov, C. W. (2009). The ArsR Repressor Mediates Arsenite-Dependent Regulation of Arsenate Respiration and Detoxification Operons of Shewanella sp. Strain ANA-3. J. Bacteriol. 191: 6722-6731 [Abstract] [Full Text]  
  • Baron, D., LaBelle, E., Coursolle, D., Gralnick, J. A., Bond, D. R. (2009). Electrochemical Measurement of Electron Transfer Kinetics by Shewanella oneidensis MR-1. J. Biol. Chem. 284: 28865-28873 [Abstract] [Full Text]  
  • Schoepp-Cothenet, B., Lieutaud, C., Baymann, F., Vermeglio, A., Friedrich, T., Kramer, D. M., Nitschke, W. (2009). Menaquinone as pool quinone in a purple bacterium. Proc. Natl. Acad. Sci. USA 106: 8549-8554 [Abstract] [Full Text]  
  • Murphy, J. N., Durbin, K. J., Saltikov, C. W. (2009). Functional Roles of arcA, etrA, Cyclic AMP (cAMP)-cAMP Receptor Protein, and cya in the Arsenate Respiration Pathway in Shewanella sp. Strain ANA-3. J. Bacteriol. 191: 1035-1043 [Abstract] [Full Text]  
  • Malasarn, D., Keeffe, J. R., Newman, D. K. (2008). Characterization of the Arsenate Respiratory Reductase from Shewanella sp. Strain ANA-3. J. Bacteriol. 190: 135-142 [Abstract] [Full Text]  


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