Abstract
Plants, cyanobacteria, and algae generate a surplus of redox power through photosynthesis, which makes them attractive for biotechnological exploitations. While central metabolism consumes most of the energy, pathways introduced through metabolic engineering can also tap into this source of reducing power. Recent work on the metabolic engineering of photosynthetic organisms has shown that the electron carriers such as ferredoxin and flavodoxin can be used to couple heterologous enzymes to photosynthetic reducing power. Because these proteins have a plethora of interaction partners and rely on electrostatically steered complex formation, they form productive electron transfer complexes with non-native enzymes. A handful of examples demonstrate channeling of photosynthetic electrons to drive the activity of heterologous enzymes, and these focus mainly on hydrogenases and cytochrome P450s. However, competition from native pathways and inefficient electron transfer rates present major obstacles, which limit the productivity of heterologous reactions coupled to photosynthesis. We discuss specific approaches to address these bottlenecks and ensure high productivity of such enzymes in a photosynthetic context.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdel-Ghany SE (2009) Contribution of plastocyanin isoforms to photosynthesis and copper homeostasis in Arabidopsis thaliana grown at different copper regimes. Planta 229:767–779. doi:10.1007/s00425-008-0869-z
Ago H, Adachi H, Umena Y et al (2016) Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga. J Biol Chem. doi:10.1074/jbc.M115.711689
Antal TK, Kovalenko IB, Rubin AB, Tyystjärvi E (2013) Photosynthesis-related quantities for education and modeling. Photosynth Res 117:1–30. doi:10.1007/s11120-013-9945-8
Atkinson JT, Campbell I, Bennett GN, Silberg JJ (2016) Cellular assays for ferredoxins: a strategy for understanding electron flow through protein carriers that link metabolic pathways. Biochemistry. doi:10.1021/acs.biochem.6b00831
Backhausen JE, Kitzmann C, Horton P, Scheibe R (2000) Electron acceptors in isolated intact spinach chloroplasts act hierarchically to prevent over-reduction and competition for electrons. Photosynth Res 64:1–13. doi:10.1023/A:1026523809147
Baebprasert W, Jantaro S, Khetkorn W et al (2011) Increased H2 production in the cyanobacterium Synechocystis sp. strain PCC 6803 by redirecting the electron supply via genetic engineering of the nitrate assimilation pathway. Metab Eng 13:610–616. doi:10.1016/j.ymben.2011.07.004
Baker NA, Sept D, Joseph S et al (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci 98:10037–10041. doi:10.1073/pnas.181342398
Berepiki A, Hitchcock A, Moore CM, Bibby TS (2016) Tapping the unused potential of photosynthesis with a heterologous electron sink. ACS Synth Biol. doi:10.1021/acssynbio.6b00100
Berry S, Schneider D, Vermaas WFJ, Rögner M (2002) Electron transport routes in whole cells of Synechocystis sp. strain PCC 6803: the role of the cytochrome bd-type oxidase. BioChemistry 41:3422–3429. doi:10.1021/bi011683d
Berthold DA, Stenmark P (2003) Membrane-bound diiron carboxylate proteins. Annu Rev Plant Biol 54:497–517. doi:10.1146/annurev.arplant.54.031902.134915
Bottin H, Lagoutte B (1992) Ferrodoxin and flavodoxin from the cyanobacterium Synechocystis sp. PCC 6803. Biochim Biophys Acta 1101:48–56. doi:10.1016/0167-4838(92)90465-P
Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318:322–373. doi:10.1016/S0005-2728(96)00112-0
Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220. doi:10.1146/annurev.arplant.56.032604.144246
Caetano-Anollés G, Kim HS, Mittenthal JE (2007) The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture. Proc Natl Acad Sci USA 104:9358–9363. doi:10.1073/pnas.0701214104
Cammack R, Rao KK, Bargeron CP et al (1977) Midpoint redox potentials of plant and algal ferredoxins. Biochem J 168:205–209
Carol P, Kuntz M (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci 6:31–36. doi:10.1016/S1360-1385(00)01811-2
Cassier-Chauvat C, Chauvat F (2014) Function and regulation of ferredoxins in the cyanobacterium, Synechocystis PCC6803: recent advances. Life 4:666–680. doi:10.3390/life4040666
Champigny ML (1995) Integration of photosynthetic carbon and nitrogen metabolism in higher plants. Photosynth Res 46:117–127. doi:10.1007/BF00020422
Cho YS, Wang QJ, Krogmann D, Whitmarsh J (1999) Extinction coefficients and midpoint potentials of cytochrome c6 from the cyanobacteria Arthrospira maxima, Microcystis aeruginosa, and Synechocystis 6803. Biochim Biophys Acta 1413:92–97. doi:10.1016/S0005-2736(99)00124-8
Clarke AK, Campbell D (1996) Inactivation of the petE Gene for plastocyanin lowers photosynthetic capacity and exacerbates chilling-induced photoinhibition in the cyanobacterium Synechococcus. Plant Physiol 112:1551–1561. doi:10.1104/pp.112.4.1551
Crowley PB, Carrondo MA (2004) The architecture of the binding site in redox protein complexes: implications for fast dissociation. Proteins Struct Funct Genet 55:603–612. doi:10.1002/prot.20043
Crowley PB, Ubbink M (2003) Close encounters of the transient kind: protein interactions in the photosynthetic redox chain investigated by NMR spectroscopy. Acc Chem Res 36:723–730. doi:10.1021/ar0200955
Dai S (2000) Redox signaling in chloroplasts: cleavage of disulfides by an iron-sulfur cluster. Science 287:655–658. doi:10.1126/science.287.5453.655
Dalby PA (2014) The role of directed protein evolution in synthetic biology. Synth Biol 1:375. doi:10.1039/9781849737845-00079
Dammeyer T, Frankenberg-Dinkel N (2008) Function and distribution of bilin biosynthesis enzymes in photosynthetic organisms. Photochemical 7:1121–1130. doi:10.1039/b807209b
Das A, Sligar SG (2009) Modulation of the cytochrome P450 reductase redox potential by the phospholipid bilayer. BioChemistry 48:12104–12112. doi:10.1021/bi9011435
De La Rosa MA, Navarro JA, Díaz-Quintana A et al (2002) An evolutionary analysis of the reaction mechanisms of photosystem I reduction by cytochrome c6 and plastocyanin. Bioelectrochemistry 55:41–45. doi:10.1016/S1567-5394(01)00136-0
Diner BA, Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53:551–580. doi:10.1146/annurev.arplant.53.100301.135238
Dubini A, Ghirardi ML (2014) Engineering photosynthetic organisms for the production of biohydrogen. Photosynth Res. doi:10.1007/s11120-014-9991-x
Eilenberg H, Weiner I, Ben-Zvi O et al (2016) The dual effect of a ferredoxin-hydrogenase fusion protein in vivo: successful divergence of the photosynthetic electron flux towards hydrogen production and elevated oxygen tolerance. Biotechnol Biofuels 9:182. doi:10.1186/s13068-016-0601-3
Erdrich P, Knoop H, Steuer R, Klamt S (2014) Cyanobacterial biofuels: new insights and strain design strategies revealed by computational modeling. Microb Cell Fact 13:128. doi:10.1186/s12934-014-0128-x
Fasan R (2012) Tuning P450 enzymes as oxidation catalysts. ACS Catal 2:647–666. doi:10.1021/cs300001x
Fixen KR, Zheng Y, Harris DF et al (2016) Light-driven carbon dioxide reduction to methane by nitrogenase in a photosynthetic bacterium. Proc Natl Acad Sci 113:10163–10167. doi:10.1073/pnas.1611043113
Fuentes P, Zhou F, Erban A et al (2016) A new synthetic biology approach allows transfer of an entire metabolic pathway from a medicinal plant to a biomass crop. Elife 5:1–26. doi:10.7554/eLife.13664
Furukawa Y, Morishima I (2001) The role of water molecules in the association of cytochrome P450cam with putidaredoxin. An osmotic pressure study. J Biol Chem 276:12983–12990. doi:10.1074/jbc.M010217200
Gangl D, Zedler JAZ, Włodarczyk A et al (2015) Expression and membrane-targeting of an active plant cytochrome P450 in the chloroplast of the green alga Chlamydomonas reinhardtii. Phytochemistry 110:22–28. doi:10.1016/j.phytochem.2014.12.006
Gao Z, Zhao H, Li Z et al (2012) Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria. Energy Environ Sci 5:9857–9865. doi:10.1039/c2ee22675h
Gao X, Gao F, Liu D et al (2016) Engineering the methylerythritol phosphate pathway in cyanobacteria for photosynthetic isoprene production from CO2. Energy Environ Sci. doi:10.1039/C5EE03102H
Ghirardi ML, Posewitz MC, Maness P-C et al (2007) Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu Rev Plant Biol 58:71–91. doi:10.1146/annurev.arplant.58.032806.103848
Girhard M, Bakkes PJ, Mahmoud O, Urlacher VB (2015) P450 biotechnology. In: de Montellano PRO (ed) Cytochrome. Springer, Cham, pp 451–520
Gnanasekaran T, Vavitsas K, Andersen-Ranberg J et al (2015) Heterologous expression of the isopimaric acid pathway in Nicotiana benthamiana and the effect of N-terminal modifications of the involved cytochrome P450 enzyme. J Biol Eng 9:24. doi:10.1186/s13036-015-0022-z
Gnanasekaran T, Karcher D, Nielsen AZ et al (2016) Transfer of the cytochrome P450-dependent dhurrin pathway from Sorghum bicolor into Nicotiana tabacum chloroplasts for light-driven synthesis. J Exp Bot 67:2495–2506. doi:10.1093/jxb/erw067
Goñi G, Serrano A, Frago S et al (2008) Flavodoxin-mediated electron transfer from photosystem I to ferredoxin-NADP+ reductase in Anabaena: role of flavodoxin hydrophobic residues in protein–protein interactions. BioChemistry 47:1207–1217. doi:10.1021/bi7017392
Goñi G, Herguedas B, Hervás M et al (2009) Flavodoxin: a compromise between efficiency and versatility in the electron transfer from photosystem i to ferredoxin-NADP(+) reductase. Biochim Biophys Acta 1787:144–154. doi:10.1016/j.bbabio.2008.12.006
Goss T, Hanke G (2014) The end of the line: can ferredoxin and ferredoxin NADP(H) oxidoreductase determine the fate of photosynthetic electrons? Curr Protein Pept Sci 15:385–393. doi:10.2174/1389203715666140327113733
Gross EL (1993) Plastocyanin: structure and function. Photosynth Res 37:103–116. doi:10.1007/BF02187469
Gupta R, He Z, Luan S (2002) Functional relationship of cytochrome c(6) and plastocyanin in Arabidopsis. Nature 417:567–571. doi:10.1038/417567a
Hamdane D, Xia C, Im SC et al (2009) Structure and function of an NADPH-cytochrome P450 oxidoreductase in an open conformation capable of reducing cytochrome P450. J Biol Chem 284:11374–11384. doi:10.1074/jbc.M807868200
Hanke G, Mulo P (2013) Plant type ferredoxins and ferredoxin-dependent metabolism. Plant Cell Environ 36:1071–1084. doi:10.1111/pce.12046
Hanke GT, Kimata-Ariga Y, Taniguchi I, Hase T (2004) A post genomic characterization of Arabidopsis ferredoxins. Plant Physiol 134:255–264. doi:10.1104/pp.103.032755
Hanke GT, Satomi Y, Shinmura K et al (2011) A screen for potential ferredoxin electron transfer partners uncovers new, redox dependent interactions. Biochim Biophys Acta 1814:366–374. doi:10.1016/j.bbapap.2010.09.011
Hirakawa H, Nagamune T (2010) Molecular assembly of P450 with ferredoxin and ferredoxin reductase by fusion to PCNA. ChemBioChem 11:1517–1520. doi:10.1002/cbic.201000226
Hirasawa M, Tripathy JN, Somasundaram R et al (2009) The interaction of spinach nitrite reductase with ferredoxin: a site-directed mutation study. Mol Plant 2:407–415. doi:10.1093/mp/ssn098
Holden HM, Jacobson BL, Hurley JK et al (1994) Structure-function studies of [2Fe-2S] ferredoxins. J Bioenerg Biomembr 26:67–88. doi:10.1007/BF00763220
Holfgrefe S, Backhausen JE, Kitzmann C, Scheibe R (1997) Regulation of steady-state photosynthesis in isolated intact chloroplasts under constant light: responses of carbon fluxes, metabolite pools and enzyme-activation states to changes of electron pressure. Plant Cell Physiol 38:1207–1216. doi:10.1093/oxfordjournals.pcp.a029107
Hoover DM, Drennan CL, Metzger a L et al (1999) Comparisons of wild-type and mutant flavodoxins from Anacystis nidulans. Structural determinants of the redox potentials. J Mol Biol 294:725–743. doi:10.1006/jmbi.1999.3152
Howe CJ, Schlarb-Ridley BG, Wastl J et al (2006) The novel cytochrome c6 of chloroplasts: a case of evolutionary bricolage? J Exp Bot 57:13–22. doi:10.1093/jxb/erj023
Hurley JK, Tollin G, Medina M, Carlos G-M (2006) Electron transfer from ferredoxin and flavodoxin to ferredoxin:NADP+ reductase. In: Photosystem I: the light-driven plastocyanin:ferredoxin oxidoreductase. Springer, Dordrecht, pp 455–476
Iwai M, Takizawa K, Tokutsu R et al (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213. doi:10.1038/nature08885
Jensen K, Jensen PE, Møller BL (2011) Light-driven cytochrome P450 hydroxylations. ACS Chem Biol 6:533–539. doi:10.1021/cb100393j
Jensen K, Johnston JB, Montellano PRO, Møller BL (2012) Photosystem I from plants as a bacterial cytochrome P450 surrogate electron donor: terminal hydroxylation of branched hydrocarbon chains. Biotechnol Lett 34:239–245. doi:10.1007/s10529-011-0768-4
Karlusich JJP, Lodeyro AF, Carrillo N (2014) The long goodbye: the rise and fall of flavodoxin during plant evolution. J Exp Bot 65:5161–5178. doi:10.1093/jxb/eru273
Kastritis PL, Moal IH, Hwang H et al (2011) A structure-based benchmark for protein-protein binding affinity. Protein Sci 20:482–491. doi:10.1002/pro.580
Kerfeld CA, Krogmann DW (1998) Photosynthetic cytochromes c in cyanobacteria, algae, and plants. Annu Rev Plant Physiol 49:397–425. doi:10.1146/annurev.arplant.49.1.397
Kim J, DellaPenna D (2006) Defining the primary route for lutein synthesis in plants: the role of Arabidopsis carotenoid beta-ring hydroxylase CYP97A3. Proc Natl Acad Sci USA 103:3474–3479. doi:10.1073/pnas.0511207103
Kim J-E, Cheng KM, Craft NE et al (2010) Over-expression of Arabidopsis thaliana carotenoid hydroxylases individually and in combination with a β-carotene ketolase provides insight into in vivo functions. Phytochemistry 71:168–178. doi:10.1016/j.phytochem.2009.10.011
Kinoshita M, yaen Kim J, Kume S et al (2015) Physicochemical nature of interfaces controlling ferredoxin NADP+ reductase activity through its interprotein interactions with ferredoxin. Biochim Biophys Acta 1847:1200–1211. doi:10.1016/j.bbabio.2015.05.023
Knaff DB, Hirasawa M (1991) Ferredoxin-dependent chloroplast enzymes. Biochim Biophys Acta 1056:93–125. doi:10.1016/S0005-2728(05)80277-4
Köninger K, Gómez Baraibar Á, Mügge C et al (2016) Recombinant cyanobacteria for the asymmetric reduction of C=C bonds fueled by the biocatalytic oxidation of water. Angew Chem Int Ed 55:5582–5585. doi:10.1002/anie.201601200
Kramer DM, Evans JR (2011) The Importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78. doi:10.1104/pp.110.166652
Ksenzhek OS, Petrova SA, Kolodyazhny M V. (1977) Electrochemical properties of some redox indicators. Bioelectrochem Bioenerg 4:346–357. doi:10.1016/0302-4598(77)80036-6
Lacour T, Ohkawa H (1999) Engineering and biochemical characterization of the rat microsomal cytochrome P4501A1 fused to ferredoxin and ferredoxin–NADP+ reductase from plant chloroplasts. Biochim Biophys Acta 1433:87–102. doi:10.1016/S0167-4838(99)00154-5
Larom S, Salama F, Schuster G, Adir N (2010) Engineering of an alternative electron transfer path in photosystem II. Proc Natl Acad Sci USA 107:9650–9655. doi:10.1073/pnas.1000187107
Larom S, Kallmann D, Saper G et al (2015) The photosystem II D1-K238E mutation enhances electrical current production using cyanobacterial thylakoid membranes in a bio-photoelectrochemical cell. Photosynth Res 126:161–169. doi:10.1007/s11120-015-0075-3
Lassen LM, Nielsen AZ, Olsen CE et al (2014a) Anchoring a plant cytochrome P450 via PsaM to the thylakoids in Synechococcus sp. PCC 7002: evidence for light-driven biosynthesis. PLoS One 9:e102184. doi:10.1371/journal.pone.0102184
Lassen LM, Nielsen AZ, Ziersen B et al (2014b) Redirecting photosynthetic electron flow into light-driven synthesis of alternative products including high-value bioactive natural compounds. ACS Synth Biol 3:1–12. doi:10.1021/sb400136f
Lee YH, Ikegami T, Standley DM et al (2011) Binding energetics of ferredoxin-NADP+ reductase with ferredoxin and its relation to function. ChemBioChem 12:2062–2070. doi:10.1002/cbic.201100189
Lemaire SD, Michelet L, Zaffagnini M et al (2007) Thioredoxins in chloroplasts. Curr Genet 51:343–365. doi:10.1007/s00294-007-0128-z
Leonard E, Koffas MAG (2007) Engineering of artificial plant cytochrome P450 enzymes for synthesis of isoflavones by Escherichia coli. Appl Environ Microbiol 73:7246–7251. doi:10.1128/AEM.01411-07
Lewis JC, Arnold FH (2009) Catalysts on demand: selective oxidations by laboratory-evolved cytochrome P450 BM3. Chim Int J Chem 63:309–312. doi:10.2533/chimia.2009.309
Marcus RA (1992) Electron transfer reactions in chemistry: theory and experiment. Rev Mod Phys. doi:10.1103/RevModPhys.65.599
Matsumura T, Sakakibara H, Nakano R et al (1997) A nitrate-inducible ferredoxin in maize roots. Genomic organization and differential expression of two nonphotosynthetic ferredoxin isoproteins. Plant Physiol 114:653–660. doi:10.1104/pp.114.2.653
Matsumura T, Kimata-Ariga Y, Sakakibara H et al (1999) Complementary DNA cloning and characterization of ferredoxin localized in bundle-sheath cells of maize leaves. Plant Physiol 119:481–488. doi:10.1104/pp.119.2.481
Mazor Y, Borovikova A, Nelson N (2015) The structure of plant photosystem I super-complex at 2.8 Å resolution. Elife 4:58–63. doi:10.7554/eLife.07433
Medina M (2009) Structural and mechanistic aspects of flavoproteins: photosynthetic electron transfer from photosystem I to NADP+. FEBS J 276:3942–3958. doi:10.1111/j.1742-4658.2009.07122.x
Mellor SB, Nielsen AZ, Burow M et al (2016) Fusion of ferredoxin and cytochrome P450 enables direct light-driven biosynthesis. ACS Chem Biol 11:1862–1869. doi:10.1021/acschembio.6b00190
Meyer Y, Buchanan BB, Vignols F, Reichheld J-P (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43:335–367. doi:10.1146/annurev-genet-102108-134201
Moal G, Lagoutte B (2012) Photo-induced electron transfer from photosystem I to NADP+: characterization and tentative simulation of the in vivo environment. Biochim Biophys Acta 1817:1635–1645. doi:10.1016/j.bbabio.2012.05.015
Molina-Heredia FP, Wastl J, Navarro JA et al (2003) A new function for an old cytochrome? Nature 424:33–34. doi:10.1038/424033b
Munro AW, Leys DG, McLean KJ et al (2002) P450 BM3: the very model of a modern flavocytochrome. Trends Biochem Sci 27:250–257. doi:10.1016/S0968-0004(02)02086-8
Munro AW, Girvan HM, McLean KJ (2007a) Cytochrome P450-redox partner fusion enzymes. Biochim Biophys Acta 1770:345–359. doi:10.1016/j.bbagen.2006.08.018
Munro AW, Girvan HM, McLean KJ (2007b) Variations on a (t)heme—novel mechanisms, redox partners and catalytic functions in the cytochrome P450 superfamily. Nat Prod Rep 24:585–609. doi:10.1039/B604190F
Munro AW, Girvan HM, Mason AE et al (2013) What makes a P450 tick? Trends Biochem Sci 38:140–150. doi:10.1016/j.tibs.2012.11.006
Murataliev MB, Feyereisen R, Walker FA (2004) Electron transfer by diflavin reductases. Biochim Biophys Acta 1698:1–26. doi:10.1016/j.bbapap.2003.10.003
Nebert DW, Wikvall K, Miller WL (2013) Human cytochromes P450 in health and disease. Philos Trans R Soc B 368:20120431–20120431. doi:10.1098/rstb.2012.0431
Nelson N, Yocum CF (2006) Structure and function of photosystems I and II. Annu Rev Plant Biol 57:521–565. doi:10.1146/annurev.arplant.57.032905.105350
Nielsen AZ, Ziersen B, Jensen K et al (2013) Redirecting photosynthetic reducing power toward bioactive natural product synthesis. ACS Synth Biol 2:308–315. doi:10.1021/sb300128r
Nielsen AZ, Mellor SB, Vavitsas K et al (2016) Extending the biosynthetic repertoires of cyanobacteria and chloroplasts. Plant J 87:87–102. doi:10.1111/tpj.13173
Northrup SH, Erickson HP (1992) Kinetics of protein-protein association explained by Brownian dynamics computer simulation. Proc Natl Acad Sci USA 89:3338–3342. doi:10.1073/pnas.89.8.3338
Oliver JWK, Atsumi S (2014) Metabolic design for cyanobacterial chemical synthesis. Photosynth Res 120:249–261. doi:10.1007/s11120-014-9997-4
Oliver JWK, Machado IMP, Yoneda H, Atsumi S (2013) Cyanobacterial conversion of carbon dioxide to 2,3-butanediol. Proc Natl Acad Sci USA 110:1249–1254. doi:10.1073/pnas.1213024110
Onda Y, Matsumura T, Kimata-ariga Y et al (2000) Differential interaction of maize root ferredoxin: NADP+ oxidoreductase with photosynthetic and non-photosynthetic ferredoxin isoproteins. Plant Physiol 123:1037–1045
Paddon CJ, Keasling JD (2014) Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development. Nat Rev Micro 12:355–367. doi:10.1038/nrmicro3240
Page CC, Moser CC, Chen X, Dutton PL (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402:47–52. doi:10.1038/46972
Page CC, Moser CC, Dutton PL (2003) Mechanism for electron transfer within and between proteins. Curr Opin Chem Biol 7:551–556. doi:10.1016/j.cbpa.2003.08.005
Pateraki I, Heskes AM, Hamberger B (2015) Cytochromes P450 for terpene functionalisation and metabolic engineering. Adv Biochem Eng Biotechnol 148:107–139. doi:10.1007/10_2014_301
Peden EA, Boehm M, Mulder DW et al (2013) Identification of global ferredoxin interaction networks in Chlamydomonas reinhardtii. J Biol Chem 288:35192–35209. doi:10.1074/jbc.M113.483727
Pinto TS, Malcata FX, Arrabaça JD et al (2013) Rubisco mutants of Chlamydomonas reinhardtii enhance photosynthetic hydrogen production. Appl Microbiol Biotechnol 97:5635–5643. doi:10.1007/s00253-013-4920-z
Porter TD (1991) An unusual yet strongly conserved flavoprotein reductase in bacteria and mammals. Trends Biochem Sci 16:154–158. doi:10.1016/0968-0004(91)90059-5
Porter TD, Kasper CB (1986) NADPH-cytochrome P-450 oxidoreductase: flavin mononucleotide and flavin adenine dinucleotide domains evolved from different flavoproteins. BioChemistry 25:1682–1687. doi:10.1021/bi00355a036
Puthiyaveetil S, Kavanagh TA, Cain P et al (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc Natl Acad Sci USA 105:10061–10066. doi:10.1073/pnas.0803928105
Raleiras P, Khanna N, Miranda H et al (2016) Turning around the electron flow in an uptake hydrogenase. EPR spectroscopy and in vivo activity of a designed mutant in HupSL from Nostoc punctiforme. Energy Environ Sci 9:581–594. doi:10.1039/C5EE02694F
Reddy VS, Giesing H a, Morton RT et al (1998) Energetics of quasiequivalence: computational analysis of protein–protein interactions in icosahedral viruses. Biophys J 74:546–558. doi:10.1016/S0006-3495(98)77813-0
Redinbo MR, Yeates TO, Merchant S (1994) Plastocyanin: Structural and functional analysis. J Bioenerg Biomembr 26:49–66. doi:10.1007/BF00763219
Reinbothe C, Bartsch S, Eggink LL et al (2006) A role for chlorophyllide a oxygenase in the regulated import and stabilization of light-harvesting chlorophyll a/b proteins. Proc Natl Acad Sci USA 103:4777–4782. doi:10.1073/pnas.0511066103
Renault H, Bassard J, Hamberger B, Werck-Reichhart D (2014) Cytochrome P450-mediated metabolic engineering: current progress and future challenges. Curr Opin Plant Biol 19:27–34. doi:10.1016/j.pbi.2014.03.004
Rintamaki E, Martinsuo P, Pursiheimo S, Aro EM (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97:11644–11649. doi:10.1073/pnas.180054297
Rittle J, Green MT (2010) Cytochrome P450 compound I: capture, characterization, and C-H bond activation kinetics. Science 330:933–937. doi:10.1126/science.1193478
Sanderson DG, Anderson LB, Gross EL (1986) Determination of the redox potential and diffusion coefficient of the protein plastocyanin using optically transparent filar electrodes. Biochim Biophys Acta 852:269–278. doi:10.1016/0005-2728(86)90232-X
Sandmann G (1986) Formation of plastocyanin and cytochrome c-553 in different species of blue-green algae. Arch Microbiol 145:76–79. doi:10.1007/BF00413030
Saxena B, Subramaniyan M, Malhotra K et al (2014) Metabolic engineering of chloroplasts for artemisinic acid biosynthesis and impact on plant growth. J Biosci 39:33–41. doi:10.1007/s12038-013-9402-z
Scheibe R, Dietz K-J (2012) Reduction-oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant Cell Environ 35:202–216. doi:10.1111/j.1365-3040.2011.02319.x
Seefeldt LC, Yang ZY, Duval S, Dean DR (2013) Nitrogenase reduction of carbon-containing compounds. Biochim Biophys Acta 1827:1102–1111. doi:10.1016/j.bbabio.2013.04.003
Sétif P (2006) Electron transfer from the bound iron–sulfur clusters to ferredoxin/flavodoxin: kinetic and structural properties of ferredoxin/flavodoxin reduction by photosystem I. In: Photosystem I. Springer, Dordrecht, pp 439–454
Shabestary K, Hudson EP (2016) Computational metabolic engineering strategies for growth-coupled biofuel production by Synechocystis. Metab Eng Commun 3:216–226. doi:10.1016/j.meteno.2016.07.003
Sheinerman F, Norel R, Honig B (2000) Electrostatic aspects of protein–protein interactions. Curr Opin Struct Biol 10:153–159. doi:10.1016/S0959-440X(00)00065-8
Simtchouk S, Eng JL, Meints CE et al (2013) Kinetic analysis of cytochrome P450 reductase from Artemisia annua reveals accelerated rates of NADH-dependent flavin reduction. FEBS J 280:6627–6642. doi:10.1111/febs.12567
Sono M, Roach MP, Coulter ED, Dawson JH (1996) Heme-containing oxygenases. Chem Rev 96:2841–2888. doi:10.1021/cr9500500
Steccanella V, Hansson M, Jensen PE (2015) Linking chlorophyll biosynthesis to a dynamic plastoquinone pool. Plant Physiol Biochem 97:207–216. doi:10.1016/j.plaphy.2015.10.009
Steinbeck J, Nikolova D, Weingarten R et al (2015) Deletion of proton gradient regulation 5 (PGR5) and PGR5-Like 1 (PGRL1) proteins promote sustainable light-driven hydrogen production in Chlamydomonas reinhardtii due to increased PSII activity under sulfur deprivation. Front Plant Sci 6:1–11. doi:10.3389/fpls.2015.00892
Stenbaek A, Jensen PE (2010) Redox regulation of chlorophyll biosynthesis. Phytochemistry 71:853–859. doi:10.1016/j.phytochem.2010.03.022
Sticht H, Rösch P (1998) The structure of iron-sulfur proteins. Prog Biophys Mol Biol 70:95–136. doi:10.1016/S0079-6107(98)00027-3
Tagawa K, Arnon DI (1968) Oxidation-reduction potentials and stoichiometry of electron transfer in ferredoxins. Biochim Biophys Acta 153:602–613. doi:10.1016/0005-2728(68)90188-6
Terauchi AM, Lu S-F, Zaffagnini M et al (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284:25867–25878. doi:10.1074/jbc.M109.023622
Tian L, Musetti V, Kim J et al (2004) The Arabidopsis LUT1 locus encodes a member of the cytochrome P450 family that is required for carotenoid-ring hydroxylation activity. Proc Natl Acad Sci 101:402–407. doi:10.1073/pnas.2237237100
Ullmann GM, Hauswald M, Jensen A, Knapp EW (2000) Structural alignment of ferredoxin and flavodoxin based on electrostatic potentials: Implications for their interactions with photosystem I and ferredoxin-NADP reductase. Proteins Struct Funct Genet 38:301–309
Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60. doi:10.1038/nature09913
Vermilion JL, Ballou DP, Massey V, Coon MJ (1981) Separate roles for FMN and FAD in catalysis by liver microsomal NADPH-cytochrome P-450 reductase. J Biol Chem 256:266–277
Wang M, Roberts DL, Paschke R et al (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc Natl Acad Sci 94:8411–8416. doi:10.1073/pnas.94.16.8411
Wastl J, Bendall DS, Howe CJ (2002) Higher plants contain a modified cytochrome c6. Trends Plant Sci 7:244–245. doi:10.1016/S1360-1385(02)02280-X
Weigel M, Varotto C, Pesaresi P et al (2003) Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 278:31286–31289. doi:10.1074/jbc.M302876200
Witt HT (1996) Primary reactions of oxygenic photosynthesis. Berichte der Bunsengesellschaft für Phys Chemie 100:1923–1942. doi:10.1002/bbpc.19961001202
Wlodarczyk A, Gnanasekaran T, Nielsen AZ et al (2016) Metabolic engineering of light-driven cytochrome P450 dependent pathways into Synechocystis sp. PCC 6803. Metab Eng 33:1–11. doi:10.1016/j.ymben.2015.10.009
Yacoby I, Pochekailov S, Toporik H et al (2011) Photosynthetic electron partitioning between [FeFe]-hydrogenase and ferredoxin:NADP+-oxidoreductase (FNR) enzymes in vitro. Proc Natl Acad Sci USA 108:9396–9401. doi:10.1073/pnas.1103659108
Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol. doi:10.1146/annurev-arplant-043015-112002
Yang Z-Y, Moure VR, Dean DR, Seefeldt LC (2012) Carbon dioxide reduction to methane and coupling with acetylene to form propylene catalyzed by remodeled nitrogenase. Proc Natl Acad Sci 109:19644–19648. doi:10.1073/pnas.1213159109
Yonekura-Sakakibara K, Onda Y, Ashikari T et al (2000) Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122:887–894. doi:10.1104/pp.122.3.887
Yoshida K, Hisabori T (2016) Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability. Proc Natl Acad Sci. doi:10.1073/pnas.1604101113
Zhang L, Pakrasi HB, Whitmarsh J (1994) Photoautotrophic growth of the cyanobacterium Synechocystis sp. PCC 6803 in the absence of cytochrome c553 and plastocyanin. J Biol Chem 269:5036–5042
Zhang J, Lu X, Li J-J (2013) Conversion of fatty aldehydes into alk (a/e)nes by in vitro reconstituted cyanobacterial aldehyde-deformylating oxygenase with the cognate electron transfer system. Biotechnol Biofuels 6:86. doi:10.1186/1754-6834-6-86
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mellor, S.B., Vavitsas, K., Nielsen, A.Z. et al. Photosynthetic fuel for heterologous enzymes: the role of electron carrier proteins. Photosynth Res 134, 329–342 (2017). https://doi.org/10.1007/s11120-017-0364-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-017-0364-0