Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria
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, whic...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-02-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/71339 |
| _version_ | 1811200428266749952 |
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| author | Yingying Wang Xi Chen Katharina Spengler Karoline Terberger Marko Boehm Jens Appel Thomas Barske Stefan Timm Natalia Battchikova Martin Hagemann Kirstin Gutekunst |
| author_facet | Yingying Wang Xi Chen Katharina Spengler Karoline Terberger Marko Boehm Jens Appel Thomas Barske Stefan Timm Natalia Battchikova Martin Hagemann Kirstin Gutekunst |
| author_sort | Yingying Wang |
| collection | DOAJ |
| description | 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)- 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, the utilization of NAD(P)H could also have been favored due to a higher competitiveness because of an accelerated metabolism. |
| first_indexed | 2024-04-12T02:04:27Z |
| format | Article |
| id | doaj.art-6df5aab1c3064084b84f7f3be2443d27 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:04:27Z |
| publishDate | 2022-02-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj.art-6df5aab1c3064084b84f7f3be2443d272022-12-22T03:52:34ZengeLife Sciences Publications LtdeLife2050-084X2022-02-011110.7554/eLife.71339Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteriaYingying Wang0https://orcid.org/0000-0002-0603-6691Xi Chen1Katharina Spengler2Karoline Terberger3Marko Boehm4Jens Appel5Thomas Barske6Stefan Timm7https://orcid.org/0000-0003-3105-6296Natalia Battchikova8Martin Hagemann9Kirstin Gutekunst10https://orcid.org/0000-0003-4366-423XDepartment of Biology, Botanical Institute, Christian-Albrechts-University, Kiel, GermanyDepartment of Biology, Botanical Institute, Christian-Albrechts-University, Kiel, GermanyDepartment of Biology, Botanical Institute, Christian-Albrechts-University, Kiel, GermanyDepartment of Biology, Botanical Institute, Christian-Albrechts-University, Kiel, GermanyDepartment of Biology, Botanical Institute, Christian-Albrechts-University, Kiel, Germany; Department of Molecular Plant Physiology, Bioenergetics in Photoautotrophs, University of Kassel, Kassel, GermanyDepartment of Biology, Botanical Institute, Christian-Albrechts-University, Kiel, Germany; Department of Molecular Plant Physiology, Bioenergetics in Photoautotrophs, University of Kassel, Kassel, GermanyPlant Physiology Department, University of Rostock, Rostock, GermanyPlant Physiology Department, University of Rostock, Rostock, GermanyDepartment of Biochemistry, Molecular Plant Biology, University of Turku, Turku, FinlandPlant Physiology Department, University of Rostock, Rostock, GermanyDepartment of Biology, Botanical Institute, Christian-Albrechts-University, Kiel, Germany; Department of Molecular Plant Physiology, Bioenergetics in Photoautotrophs, University of Kassel, Kassel, GermanyThe 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)- 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, the utilization of NAD(P)H could also have been favored due to a higher competitiveness because of an accelerated metabolism.https://elifesciences.org/articles/71339Synechocystis sp. PCC 6803ferredoxinpyruvate dehydrogenasecyanobacteriaGOGATPFOR |
| spellingShingle | Yingying Wang Xi Chen Katharina Spengler Karoline Terberger Marko Boehm Jens Appel Thomas Barske Stefan Timm Natalia Battchikova Martin Hagemann Kirstin Gutekunst Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria eLife Synechocystis sp. PCC 6803 ferredoxin pyruvate dehydrogenase cyanobacteria GOGAT PFOR |
| title | Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria |
| title_full | Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria |
| title_fullStr | Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria |
| title_full_unstemmed | Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria |
| title_short | Pyruvate:ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria |
| title_sort | pyruvate ferredoxin oxidoreductase and low abundant ferredoxins support aerobic photomixotrophic growth in cyanobacteria |
| topic | Synechocystis sp. PCC 6803 ferredoxin pyruvate dehydrogenase cyanobacteria GOGAT PFOR |
| url | https://elifesciences.org/articles/71339 |
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