Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria
- Christian-Albrechts University, Germany
- University of Kassel, Germany
- University of Rostock, Germany
- University of Turku, Finland
Abstract
The decarboxylation of pyruvate is a central reaction in the carbon metabolism of all organisms. It is catalyzed by the pyruvate:ferredoxin oxidoreductase (PFOR) and the pyruvate dehydrogenase (PDH) complex. Whereas PFOR reduces ferredoxin, the PDH complex utilizes NAD+. Anaerobes rely on PFOR, which was replaced during evolution by the PDH complex found in aerobes. Cyanobacteria possess both enzyme systems. Our data challenge the view that PFOR is exclusively utilized for fermentation. Instead, we show, that the cyanobacterial PFOR is stable in the presence of oxygen in vitro and is required for optimal photomixotrophic growth under aerobic and highly reducing conditions while the PDH complex is inactivated. We found that cells rely on a general shift from utilizing NAD(H)-dependent to ferredoxin-dependent enzymes under these conditions. The utilization of ferredoxins instead of NAD(H) saves a greater share of the Gibbs free energy, instead of wasting it as heat. This obviously simultaneously decelerates metabolic reactions as they operate closer to their thermodynamic equilibrium. It is common thought that during evolution, ferredoxins were replaced by NAD(P)H due to their higher stability in an oxidizing atmosphere. However, utilization of NAD(P)H could also have been favored due to a higher competitiveness because of an accelerated metabolism.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 1,2, 3 and Figures supplement 1,2,3,4,5,6,7,8 as mentioned in the transparent report.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (DFG Gu1522/2-1)
- Kirstin Gutekunst
Chinese Government Scholarship (201406320187)
- Yingying Wang
Deutsche Forschungsgemeinschaft (HA2002/23-1)
- Thomas Barske
Deutsche Forschungsgemeinschaft (FOR2816)
- Martin Hagemann
- Kirstin Gutekunst
Bundesministerium für Bildung und Forschung (BMBF FP309)
- Marko Boehm
- Jens Appel
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2022, Wang et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria
eLife 11:e71339.
https://doi.org/10.7554/eLife.71339
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