AEM Accepts, published online ahead of print on 6 November 2009

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Appl. Environ. Microbiol. doi:10.1128/AEM.01854-09
Copyright (c) 2009, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Evaluation of Oxygen Metabolism in Anaeromyxobacter dehalogenans Strain 2CP-C Reveals Unique Ecophysiology Among U(VI)-Reducing Bacteria

Sara H. Thomas, Robert A. Sanford, Benjamin K. Amos, Mary Beth Leigh, Erick Cardenas, and Frank E. Löffler^*

School of Civil and Environmental Engineering, School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332-0512; Department of Geology, University of Illinois, Urbana, Illinois 61801-2352; Department of Biology and Wildlife and Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska 99775; Center for Microbial Ecology, Michigan State University, East Lansing, Michigan 48824

^* To whom correspondence should be addressed. Email: frank.loeffler{at}ce.gatech.edu.

Anaeromyxobacter spp. respire soluble hexavalent uranium, U(VI), leading to the formation of insoluble U(IV), and are present at the uranium-contaminated Oak Ridge Integrated Field Research Challenge (IFC) site. Pilot-scale in situ bioreduction of U(VI) has been accomplished in Area 3 of the Oak Ridge IFC site following biostimulation, but the susceptibility of the reduced material to oxidants (i.e., oxygen) compromises long-term U immobilization. Following oxygen intrusion, attached A. dehalogenans cells increased approximately five-fold from 2.2 x 10⁷ ± 8.6 x 10⁶ to 1.0 x 10⁸ ± 2.2 x 10⁷ cells per g of sediment collected from well FW101-2. In the same samples, cell numbers of Geobacter lovleyi, a population native to Area 3 and also capable of U(VI) reduction, decreased or did not change. A. dehalogenans cells captured via groundwater sampling (i.e., not attached to sediment) were present in much lower numbers (<1.3 x 10⁴ ± 1.1 x 10⁴ cells per L) than sediment-associated cells, suggesting that A. dehalogenans cells occur predominantly in association with soil particles. Laboratory studies confirmed aerobic growth of A. dehalogenans strain 2CP-C at initial oxygen partial pressures (pO₂) at and below 0.18 atm. A negative linear correlation (μ = -0.09 x pO₂ + 0.051; R² = 0.923) was observed between the instantaneous specific growth rate μ and pO₂, indicating that this organism should be classified as a microaerophile. Quantification of cells during aerobic growth revealed that the fraction of electrons released in electron donor oxidation and used for biomass production (f_s) decreased from 0.52 at a pO₂ of 0.02 atm to 0.19 at a pO₂ of 0.18 atm. Hence, the apparent fraction of electrons utilized for energy generation (i.e., oxygen reduction) (f_e) increased from 0.48 to 0.81 with increasing pO₂, suggesting that oxygen is consumed in a non-respiratory process at high pO₂. The ability to tolerate high oxygen concentrations, microaerophilic oxygen respiration, and preferential association with soil particles represents an ecophysiology that distinguishes A. dehalogenans from other known U(VI)-reducing bacteria in Area 3, and these features may play roles for stabilizing immobilized radionuclides in situ.