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Applied and Environmental Microbiology, March 2006, p. 1988-1996, Vol. 72, No. 3
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.3.1988-1996.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Enhanced Exopolymer Production and Chromium Stabilization in Pseudomonas putida Unsaturated Biofilms

John H. Priester,¹ Scott G. Olson,¹ Samuel M. Webb,² Mary P. Neu,³ Larry E. Hersman,⁴ and Patricia A. Holden^1*

Donald Bren School of Environmental Science & Management, University of California, Santa Barbara, California 93106-5131,¹ Stanford Synchrotron Radiation Laboratory, Stanford Linear Accelerator Center, Menlo Park, California 94025,² Chemistry Division, Los Alamos National Laboratory, Los Alamos, New Mexico 87545,³ Bioscience Division, Los Alamos, National Laboratory, Los Alamos, New Mexico 87545⁴

Received 19 August 2005/ Accepted 15 December 2005

Chromium-contaminated soils threaten surface and groundwater quality at many industrial sites. In vadose zones, indigenous bacteria can reduce Cr(VI) to Cr(III), but the subsequent fate of Cr(III) and the roles of bacterial biofilms are relatively unknown. To investigate, we cultured Pseudomonas putida, a model organism for vadose zone bioremediation, as unsaturated biofilms on membranes overlaying iron-deficient solid media either containing molecular dichromate from potassium dichromate (Cr-only treatment) or with deposits of solid, dichromate-coated hematite (Fe+Cr treatment) to simulate vadose zone conditions. Controls included iron-deficient solid medium and an Fe-only treatment using solid hematite deposits. Under iron-deficient conditions, chromium exposure resulted in lower cell yield and lower amounts of cellular protein and carbohydrate, but providing iron in the form of hematite overcame these toxic effects of Cr. For the Cr and Fe+Cr treatments, Cr(VI) was completely reduced to Cr(III) that accumulated on biofilm cells and extracellular polymeric substances (EPSs). Chromium exposure resulted in elevated extracellular carbohydrates, protein, DNA, and EPS sugars that were relatively enriched in N-acetyl-glucosamine, rhamnose, glucose, and mannose. The proportions of EPS protein and carbohydrate relative to intracellular pools suggested Cr toxicity-mediated cell lysis as the origin. However, DNA accumulated extracellularly in amounts far greater than expected from cell lysis, and Cr was liberated when extracted EPS was treated with DNase. These results demonstrate that Cr accumulation in unsaturated biofilms occurs with enzymatic reduction of Cr(VI), cellular lysis, cellular association, and extracellular DNA binding of Cr(III), which altogether can facilitate localized biotic stabilization of Cr in contaminated vadose zones.

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* Corresponding author. Mailing address: University of California, Santa Barbara, Donald Bren School of Environmental Science & Management, Santa Barbara, CA 93106-5131. Phone: (805) 893-3195. Fax: (805) 893-7612. E-mail: holden{at}bren.ucsb.edu.

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Applied and Environmental Microbiology, March 2006, p. 1988-1996, Vol. 72, No. 3
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.3.1988-1996.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

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