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Applied and Environmental Microbiology, November 2003, p. 6577-6586, Vol. 69, No. 11
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.11.6577-6586.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Microaerophilic Cooperation of Reductive and Oxidative Pathways Allows Maximal Photosynthetic Membrane Biosynthesis in Rhodospirillum rubrum

Hartmut Grammel,1* Ernst-Dieter Gilles,1 and Robin Ghosh2

Max Planck Institute for Dynamics of Complex Technical Systems, D-39106 Magdeburg,1 Department of Bioenergetics, Institute for Biology, University of Stuttgart, D-70550 Stuttgart, Germany2

Received 7 April 2003/ Accepted 15 August 2003

The purple nonsulfur bacterium Rhodospirillum rubrum has been employed to study physiological adaptation to limiting oxygen tensions (microaerophilic conditions). R. rubrum produces maximal levels of photosynthetic membranes when grown with both succinate and fructose as carbon sources under microaerophilic conditions in comparison to the level (only about 20% of the maximum) seen in the absence of fructose. Employing a unique partial O2 pressure (pO2) control strategy to reliably adjust the oxygen tension to values below 0.5%, we have used bioreactor cultures to investigate the metabolic rationale for this effect. A metabolic profile of the central carbon metabolism of these cultures was obtained by determination of key enzyme activities under microaerophilic as well as aerobic and anaerobic phototrophic conditions. Under aerobic conditions succinate and fructose were consumed simultaneously, whereas oxygen-limiting conditions provoked the preferential breakdown of fructose. Fructose was utilized via the Embden-Meyerhof-Parnas pathway. High levels of pyrophosphate-dependent phosphofructokinase activity were found to be specific for oxygen-limited cultures. No glucose-6-phosphate dehydrogenase activity was detected under any conditions. We demonstrate that NADPH is supplied mainly by the pyridine-nucleotide transhydrogenase under oxygen-limiting conditions. The tricarboxylic acid cycle enzymes are present at significant levels during microaerophilic growth, albeit at lower levels than those seen under fully aerobic growth conditions. Levels of the reductive tricarboxylic acid cycle marker enzyme fumarate reductase were also high under microaerophilic conditions. We propose a model by which the primary "switching" of oxidative and reductive metabolism is performed at the level of the tricarboxylic acid cycle and suggest how this might affect redox signaling and gene expression in R. rubrum.

* Corresponding author. Mailing address: Max Planck Institute for Dynamics of Complex Technical Systems, Sandtorstr. 1, D-39106 Magdeburg, Germany. Phone: 49-391-6110-255. Fax: 49-391-6110-527. E-mail: grammel{at}mpi-magdeburg.mpg.de.

Applied and Environmental Microbiology, November 2003, p. 6577-6586, Vol. 69, No. 11
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.11.6577-6586.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Grammel, H., Ghosh, R. (2008). Redox-State Dynamics of Ubiquinone-10 Imply Cooperative Regulation of Photosynthetic Membrane Expression in Rhodospirillum rubrum. J. Bacteriol. 190: 4912-4921 [Abstract] [Full Text]  
  • Lupo, D., Ghosh, R. (2004). The Reaction Center H Subunit Is Not Required for High Levels of Light-Harvesting Complex 1 in Rhodospirillum rubrum Mutants. J. Bacteriol. 186: 5585-5595 [Abstract] [Full Text]  


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