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Journal of Bacteriology, June 2007, p. 3935-3944, Vol. 189, No. 11
0021-9193/07/$08.00+0     doi:10.1128/JB.01861-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Transcription of All amoC Copies Is Associated with Recovery of Nitrosomonas europaea from Ammonia Starvation{triangledown}

Paul M. Berube,1 Ram Samudrala,1 and David A. Stahl1,2*

Department of Microbiology, University of Washington,1 Department of Civil and Environmental Engineering, University of Washington, Seattle, Washington2

Received 11 December 2006/ Accepted 14 March 2007

The chemolithotrophic ammonia-oxidizing bacterium Nitrosomonas europaea is known to be highly resistant to starvation conditions. The transcriptional response of N. europaea to ammonia addition following short- and long-term starvation was examined by primer extension and S1 nuclease protection analyses of genes encoding enzymes for ammonia oxidation (amoCAB operons) and CO2 fixation (cbbLS), a third, lone copy of amoC (amoC3), and two representative housekeeping genes (glyA and rpsJ). Primer extension analysis of RNA isolated from growing, starved, and recovering cells revealed two differentially regulated promoters upstream of the two amoCAB operons. The distal {sigma}70 type amoCAB promoter was constitutively active in the presence of ammonia, but the proximal promoter was only active when cells were recovering from ammonia starvation. The lone, divergent copy of amoC (amoC3) was expressed only during recovery. Both the proximal amoC1,2 promoter and the amoC3 promoter are similar to gram-negative {sigma}E promoters, thus implicating {sigma}E in the regulation of the recovery response. Although modeling of subunit interactions suggested that a nonconservative proline substitution in AmoC3 may modify the activity of the holoenzyme, characterization of a {Delta}amoC3 strain showed no significant difference in starvation recovery under conditions evaluated. In contrast to the amo transcripts, a delayed appearance of transcripts for a gene required for CO2 fixation (cbbL) suggested that its transcription is retarded until sufficient energy is available. Overall, these data revealed a programmed exit from starvation likely involving regulation by {sigma}E and the coordinated regulation of catabolic and anabolic genes.

* Corresponding author. Mailing address: Department of Civil and Environmental Engineering, University of Washington, 302 More Hall, Box 352700, Seattle, WA 98195-2700. Phone: (206) 685-3464. Fax: (206) 685-9185. E-mail: dastahl{at}u.washington.edu

{triangledown} Published ahead of print on 23 March 2007.

Journal of Bacteriology, June 2007, p. 3935-3944, Vol. 189, No. 11
0021-9193/07/$08.00+0     doi:10.1128/JB.01861-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Norton, J. M., Klotz, M. G., Stein, L. Y., Arp, D. J., Bottomley, P. J., Chain, P. S. G., Hauser, L. J., Land, M. L., Larimer, F. W., Shin, M. W., Starkenburg, S. R. (2008). Complete Genome Sequence of Nitrosospira multiformis, an Ammonia-Oxidizing Bacterium from the Soil Environment. Appl. Environ. Microbiol. 74: 3559-3572 [Abstract] [Full Text]  
  • El Sheikh, A. F., Poret-Peterson, A. T., Klotz, M. G. (2008). Characterization of Two New Genes, amoR and amoD, in the amo Operon of the Marine Ammonia Oxidizer Nitrosococcus oceani ATCC 19707. Appl. Environ. Microbiol. 74: 312-318 [Abstract] [Full Text]  


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