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Applied and Environmental Microbiology, November 2009, p. 6639-6646, Vol. 75, No. 21
0099-2240/09/$08.00+0     doi:10.1128/AEM.00054-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Rhodobacter capsulatus Catalyzes Light-Dependent Fe(II) Oxidation under Anaerobic Conditions as a Potential Detoxification Mechanism{triangledown}

Alexandre J. Poulain1,{dagger} and Dianne K. Newman1,2,3*

Biaology Department, Massachusetts Institute of Technology, 68-380, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139,1 Earth, Atmospheric and Planetary Sciences Department, Massachusetts Institute of Technology, 68-380, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139,2 Howard Hughes Medical Institute, 68-380, 77 Massachusetts Avenue, Cambridge, Massachusetts 021393

Received 9 January 2009/ Accepted 22 August 2009

Diverse bacteria are known to oxidize millimolar concentrations of ferrous iron [Fe(II)] under anaerobic conditions, both phototrophically and chemotrophically. Yet whether they can do this under conditions that are relevant to natural systems is understood less well. In this study, we tested how light, Fe(II) speciation, pH, and salinity affected the rate of Fe(II) oxidation by Rhodobacter capsulatus SB1003. Although R. capsulatus cannot grow photoautotrophically on Fe(II), it oxidizes Fe(II) at rates comparable to those of bacteria that do grow photoautotrophically on Fe(II) as soon as it is exposed to light, provided it has a functional photosystem. Chelation of Fe(II) by diverse organic ligands promotes Fe(II) oxidation, and as the pH increases, so does the oxidation rate, except in the presence of nitrilotriacetate; nonchelated forms of Fe(II) are also more rapidly oxidized at higher pH. Salt concentrations typical of marine environments inhibit Fe(II) oxidation. When growing photoheterotrophically on humic substances, R. capsulatus is highly sensitive to low concentrations of Fe(II); it is inhibited in the presence of concentrations as low as 5 µM. The product of Fe(II) oxidation, ferric iron, does not hamper growth under these conditions. When other parameters, such as pH or the presence of chelators, are adjusted to promote Fe(II) oxidation, the growth inhibition effect of Fe(II) is alleviated. Together, these results suggest that Fe(II) is toxic to R. capsulatus growing under strictly anaerobic conditions and that Fe(II) oxidation alleviates this toxicity.


* Corresponding author. Mailing address: Biology Department, Massachusetts Institute of Technology, 68-380, 77 Massachusetts Avenue, Cambridge, MA 02139. Phone: (617) 324-2770. Fax: (617) 324-3972. E-mail: dkn{at}mit.edu

{triangledown} Published ahead of print on 28 August 2009.

{dagger} Present address: Biology Department, Center for Advanced Research in Environmental Genomics, University of Ottawa, 160-30 Marie Curie, Ottawa, ON, Canada K1N 6N5.


Applied and Environmental Microbiology, November 2009, p. 6639-6646, Vol. 75, No. 21
0099-2240/09/$08.00+0     doi:10.1128/AEM.00054-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.