Identification of Global Ferredoxin Interaction Networks in Chlamydomonas reinhardtii

Peden, Erin A.; Boehm, Marko; Mulder, David W.; Davis, ReAnna; Old, William M.; King, Paul W.; Ghirardi, Maria L.; Dubini, Alexandra

doi:10.1074/jbc.m113.483727

Cited by 99 publications

(107 citation statements)

References 68 publications

(56 reference statements)

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“…NADPH and NADH were both proven to donate electrons to Synechocystis Flv3 in vitro (4). However, the electron donor might also be ferredoxin, because FdxI, one of ferredoxins of Chlamydomonas reinhardtii, was recently found to interact with Flv3, a homolog of cyanobacterial-like flavodiiron proteins (27). Current knowledge of heterocyst-specific metabolism does not allow us to make a direct distinction between possible electron donors to Flv3B.…”

Section: Discussionmentioning

confidence: 99%

Heterocyst-specific flavodiiron protein Flv3B enables oxic diazotrophic growth of the filamentous cyanobacterium Anabaena sp. PCC 7120

Ermakova

Battchikova

Richaud

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Flavodiiron proteins are known to have crucial and specific roles in photoprotection of photosystems I and II in cyanobacteria. The filamentous, heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 contains, besides the four flavodiiron proteins Flv1A, Flv2, Flv3A, and Flv4 present in vegetative cells, two heterocyst-specific flavodiiron proteins, Flv1B and Flv3B. Here, we demonstrate that Flv3B is responsible for light-induced O 2 uptake in heterocysts, and that the absence of the Flv3B protein severely compromises the growth of filaments in oxic, but not in microoxic, conditions. It is further demonstrated that Flv3B-mediated photosynthetic O 2 uptake has a distinct role in heterocysts which cannot be substituted by respiratory O 2 uptake in the protection of nitrogenase from oxidative damage and, thus, in an efficient provision of nitrogen to filaments. In line with this conclusion, the Δflv3B strain has reduced amounts of nitrogenase NifHDK subunits and shows multiple symptoms of nitrogen deficiency in the filaments. The apparent imbalance of cytosolic redox state in Δflv3B heterocysts also has a pronounced influence on the amounts of different transcripts and proteins. Therefore, an O 2 -related mechanism for control of gene expression is suggested to take place in heterocysts.nitrogen fixation | oxygen protection | photosynthesis

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Section: Discussionmentioning

confidence: 99%

Heterocyst-specific flavodiiron protein Flv3B enables oxic diazotrophic growth of the filamentous cyanobacterium Anabaena sp. PCC 7120

Ermakova

Battchikova

Richaud

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…3) constitutes a major challenge. While the primary electron sinks-such as NADP + photoreductionare relatively well understood, recent proteomic studies on ferredoxin interaction partners of Synechocystis and Chlamydomonas ferredoxins have identified ~200 possible ferredoxin-dependent proteins (Hanke et al 2011;Peden et al 2013;Cassier-Chauvat and Chauvat 2014). This highlights the incompleteness of our knowledge of ferredoxin-dependent processes and underlines the importance of competitiveness for heterologous enzymes.…”

Section: Native Competition For Photosynthetic Reducing Powermentioning

confidence: 99%

Photosynthetic fuel for heterologous enzymes: the role of electron carrier proteins

et al. 2017

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“…Using a yeast two hybrid approach, a global FDX interaction network was established for Chlamydomonas, suggesting putative roles for FDX1 (originally designated Fd) in redox metabolism, carbohydrate modification, and fatty acid biosynthesis (5); this FDX was already known to function in both linear and cyclic photosynthetic electron flow (4,6). FDX1 also accepts electrons from FDX-NADP oxidoreductase (FNR) (7) and donates electrons to HYDA hydrogenases (5,8,9). Other FDXs may be involved in state transitions, nitrogen metabolism, cellular responses to reactive oxygen species (ROS), and dark anoxia (4,5,(10)(11)(12)(13).…”

mentioning

confidence: 99%

“…FDX1 also accepts electrons from FDX-NADP oxidoreductase (FNR) (7) and donates electrons to HYDA hydrogenases (5,8,9). Other FDXs may be involved in state transitions, nitrogen metabolism, cellular responses to reactive oxygen species (ROS), and dark anoxia (4,5,(10)(11)(12)(13).…”

mentioning

confidence: 99%

Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism

Yang

Wittkopp

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Photosynthetic microorganisms typically have multiple isoforms of the electron transfer protein ferredoxin, although we know little about their exact functions. Surprisingly, a Chlamydomonas reinhardtii mutant null for the ferredoxin-5 gene (FDX5) completely ceased growth in the dark, with both photosynthetic and respiratory functions severely compromised; growth in the light was unaffected. Thylakoid membranes in dark-maintained fdx5 mutant cells became severely disorganized concomitant with a marked decrease in the ratio of monogalactosyldiacylglycerol to digalactosyldiacylglycerol, major lipids in photosynthetic membranes, and the accumulation of triacylglycerol. Furthermore, FDX5 was shown to physically interact with the fatty acid desaturases CrΔ4FAD and CrFAD6, likely donating electrons for the desaturation of fatty acids that stabilize monogalactosyldiacylglycerol. Our results suggest that in photosynthetic organisms, specific redox reactions sustain dark metabolism, with little impact on daytime growth, likely reflecting the tailoring of electron carriers to unique intracellular metabolic circuits under these two very distinct redox conditions. ferredoxin | dark growth | thylakoid lipids | triacylglycerol | redox regulation F erredoxins (FDXs) are soluble, iron-sulfur proteins that mediate electron transfer in a variety of essential metabolic reactions (1-3) (SI Appendix, Fig. S1). The Chlamydomonas genome encodes 13 FDXs (SI Appendix, Table S1) with localization and redox properties that suggest involvement in specific redox reactions (4). Using a yeast two hybrid approach, a global FDX interaction network was established for Chlamydomonas, suggesting putative roles for FDX1 (originally designated Fd) in redox metabolism, carbohydrate modification, and fatty acid biosynthesis (5); this FDX was already known to function in both linear and cyclic photosynthetic electron flow (4, 6). FDX1 also accepts electrons from FDX-NADP oxidoreductase (FNR) (7) and donates electrons to HYDA hydrogenases (5,8,9). Other FDXs may be involved in state transitions, nitrogen metabolism, cellular responses to reactive oxygen species (ROS), and dark anoxia (4, 5, 10-13).The major lipids in thylakoid membranes are monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), phosphatidylglycerol (PG), and sulfoquinovosyldiacylglycerol (SQDG) (14-17), with MGDG being the most abundant, followed by DGDG (14, 17). In Arabidopsis, three enzyme systems are involved in MGDG and DGDG synthesis (18). In contrast, there is only a single copy each of an MGDG and DGDG synthase gene in Chlamydomonas (19). Chlamydomonas uses the prokaryotic pathway for thylakoid lipid synthesis (20) in which the MGDG species synthesized in chloroplasts contain predominantly C18:3 Δ9,12,15 -sn-1 with the unusual hexadeca-4, 7, 10, 13-tetraenoic acid C16:4 Δ4,7,10,13 at the sn-2 position (20). Desaturation of the sn-2 acyl group of Chlamydomonas MGDG requires the CrΔ4FAD desaturase, which is not present in Arabidopsis (21), and MGDG accumulation in...

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Identification of Global Ferredoxin Interaction Networks in Chlamydomonas reinhardtii

Cited by 99 publications

References 68 publications

Heterocyst-specific flavodiiron protein Flv3B enables oxic diazotrophic growth of the filamentous cyanobacterium Anabaena sp. PCC 7120

Heterocyst-specific flavodiiron protein Flv3B enables oxic diazotrophic growth of the filamentous cyanobacterium Anabaena sp. PCC 7120

Photosynthetic fuel for heterologous enzymes: the role of electron carrier proteins

Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism

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