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Applied and Environmental Microbiology, August 2006, p. 5578-5588, Vol. 72, No. 8
0099-2240/06/$08.00+0     doi:10.1128/AEM.00284-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Temporal Transcriptomic Analysis as Desulfovibrio vulgaris Hildenborough Transitions into Stationary Phase during Electron Donor Depletion

M. E. Clark,¹ Q. He,² Z. He,^2,8 K. H. Huang,³ E. J. Alm,³ X.-F. Wan,¹ T. C. Hazen,⁴ A. P. Arkin,^3,5,6 J. D. Wall,⁷ J.-Z. Zhou,^2,8 and M. W. Fields^1*,

Department of Microbiology, Miami University, Oxford, Ohio 45056,¹ Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831,² Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720,³ Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720,⁴ Department of Bioengineering, University of California, Berkeley, California 94720,⁵ Howard Hughes Medical Institute, Berkeley, California 94720,⁶ Department of Biochemistry, University of Missouri—Columbia, Columbia, Missouri 65211,⁷ Institute for Environmental Genomics, Department of Botany and Microbiology, University of Oklahoma, Norman, Oklahoma 73019⁸

Received 3 February 2006/ Accepted 21 May 2006

Desulfovibrio vulgaris was cultivated in a defined medium, and biomass was sampled for approximately 70 h to characterize the shifts in gene expression as cells transitioned from the exponential to the stationary phase during electron donor depletion. In addition to temporal transcriptomics, total protein, carbohydrate, lactate, acetate, and sulfate levels were measured. The microarray data were examined for statistically significant expression changes, hierarchical cluster analysis, and promoter element prediction and were validated by quantitative PCR. As the cells transitioned from the exponential phase to the stationary phase, a majority of the down-expressed genes were involved in translation and transcription, and this trend continued at the remaining times. There were general increases in relative expression for intracellular trafficking and secretion, ion transport, and coenzyme metabolism as the cells entered the stationary phase. As expected, the DNA replication machinery was down-expressed, and the expression of genes involved in DNA repair increased during the stationary phase. Genes involved in amino acid acquisition, carbohydrate metabolism, energy production, and cell envelope biogenesis did not exhibit uniform transcriptional responses. Interestingly, most phage-related genes were up-expressed at the onset of the stationary phase. This result suggested that nutrient depletion may affect community dynamics and DNA transfer mechanisms of sulfate-reducing bacteria via the phage cycle. The putative feoAB system (in addition to other presumptive iron metabolism genes) was significantly up-expressed, and this suggested the possible importance of Fe²⁺ acquisition under metal-reducing conditions. The expression of a large subset of carbohydrate-related genes was altered, and the total cellular carbohydrate levels declined during the growth phase transition. Interestingly, the D. vulgaris genome does not contain a putative rpoS gene, a common attribute of the -Proteobacteria genomes sequenced to date, and the transcription profiles of other putative rpo genes were not significantly altered. Our results indicated that in addition to expected changes (e.g., energy conversion, protein turnover, translation, transcription, and DNA replication and repair), genes related to phage, stress response, carbohydrate flux, the outer envelope, and iron homeostasis played important roles as D. vulgaris cells experienced electron donor depletion.

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* Corresponding author. Mailing address: Department of Microbiology, Miami University, Pearson Hall, Rm. 32, Oxford, OH 45056. Phone: (513) 529-5434. Fax: (513) 529-2431. E-mail: fieldsmw{at}muohio.edu.

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

All authors are affiliated with the Virtual Institute for Microbial Stress and Survival (http://vimss.lbl.gov).

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Applied and Environmental Microbiology, August 2006, p. 5578-5588, Vol. 72, No. 8
0099-2240/06/$08.00+0     doi:10.1128/AEM.00284-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

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