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Journal of Bacteriology, December 2005, p. 8437-8449, Vol. 187, No. 24
0021-9193/05/$08.00+0     doi:10.1128/JB.187.24.8437-8449.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Whole-Genome Transcriptional Analysis of Heavy Metal Stresses in Caulobacter crescentus

Ping Hu,¹ Eoin L. Brodie,¹ Yohey Suzuki,^2, Harley H. McAdams,³ and Gary L. Andersen^1*

Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, California 94720,¹ Frontier Research System for Extremophiles, Japan Marine Science & Technology Center, 2-15, Natushima-cho, Yokosuka 237-006, Japan,² Department of Developmental Biology, Stanford University, Stanford, California 94305-5329³

Received 24 June 2005/ Accepted 26 September 2005

The bacterium Caulobacter crescentus and related stalk bacterial species are known for their distinctive ability to live in low-nutrient environments, a characteristic of most heavy metal-contaminated sites. Caulobacter crescentus is a model organism for studying cell cycle regulation with well-developed genetics. We have identified the pathways responding to heavy-metal toxicity in C. crescentus to provide insights for the possible application of Caulobacter to environmental restoration. We exposed C. crescentus cells to four heavy metals (chromium, cadmium, selenium, and uranium) and analyzed genome-wide transcriptional activities postexposure using an Affymetrix GeneChip microarray. C. crescentus showed surprisingly high tolerance to uranium, a possible mechanism for which may be the formation of extracellular calcium-uranium-phosphate precipitates. The principal response to these metals was protection against oxidative stress (up-regulation of manganese-dependent superoxide dismutase sodA). Glutathione S-transferase, thioredoxin, glutaredoxins, and DNA repair enzymes responded most strongly to cadmium and chromate. The cadmium and chromium stress response also focused on reducing the intracellular metal concentration, with multiple efflux pumps employed to remove cadmium, while a sulfate transporter was down-regulated to reduce nonspecific uptake of chromium. Membrane proteins were also up-regulated in response to most of the metals tested. A two-component signal transduction system involved in the uranium response was identified. Several differentially regulated transcripts from regions previously not known to encode proteins were identified, demonstrating the advantage of evaluating the transcriptome by using whole-genome microarrays.

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

Present address: National Institute of Advanced Industrial Science and Technology (AIST), Research Center for Deep Geological Environments, AIST Tsukuba Central 7, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8567, Japan.

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