Abstract
Ferredoxins are soluble iron sulphur proteins which function as electron donors in a number of metabolic pathways in a broad range of organisms. In photosynthetic organisms, PETF, or ferredoxin 1 (FDX1), is the most studied ferredoxin due to its essential role in photosynthesis, where it transfers electrons from photosystem I to ferredoxin-NADP+ oxidoreductase. However, PETF can also transfer electrons to a large number of other proteins. One important PETF electron acceptor found in green microalgae is the biologically and biotechnologically important [FeFe]-hydrogenase HYDA, which catalyses the production of molecular hydrogen (H2) from protons and electrons. The interaction between PETF and HYDA is of considerable interest, as PETF is the primary electron donor to HYDA and electron supply is one of the main limiting factors for H2 production on a commercial scale. Although there is no three dimensional structure of the PETF–HYDA complex available, protein variants, nuclear magnetic resonance titration studies, molecular dynamics and modelling have provided considerable insight into the residues essential for forming and maintaining the interaction. In this review, we discuss the most recent findings with regard to ferredoxin-HYDA interactions and the evolution of the various Chlamydomonas reinhardtii ferredoxin isoforms. Finally, we provide an outlook on new PETF-based biotechnological approaches for improved H2 production efficiencies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baek K, Kim DH, Jeong J, Sim SJ, Melis A, Kim JS, Jin E, Bae S (2016) DNA-free two-gene knockout in Chlamydomonas reinhardtii via CRISPR-Cas9 ribonucleoproteins. Sci Rep. doi:10.1038/srep30620
Bashir Q, Scanu S, Ubbink M (2011) Dynamics in electron transfer protein complexes. FEBS J 278:1391–1400. doi:10.1111/j.1742-4658.2011.08062.x
Berg OG, Vonhippel PH (1985) Diffusion-controlled macromolecular interactions. Annu Rev Biophys Biol 14:131–160. doi:10.1146/annurev.biophys.14.1.131
Boehm M, Alahuhta M, Mulder DW, Peden EA, Long H, Brunecky R, Lunin VV, King PW, Ghirardi ML, Dubini A (2016) Crystal structure and biochemical characterization of Chlamydomonas FDX2 reveal two residues that, when mutated, partially confer FDX2 the redox potential and catalytic properties of FDX1. Photosynth Res 128:45–57. doi:10.1007/s11120-015-0198-6
Chang CH, King PW, Ghirardi ML, Kim K (2007) Atomic resolution modeling of the ferredoxin: [FeFe] hydrogenase complex from Chlamydomonas reinhardtii. Biophys J 93:3034–3045. doi:10.1529/biophysj.107.108589
Crowley PB, Ubbink M (2003) Close encounters of the transient kind: Protein interactions in the photosynthetic redox chain investigated by NMR spectroscopy. Accounts Chem Res 36:723–730. doi:10.1021/ar0200955
D’Adamo S, Jinkerson RE, Boyd ES, Brown SL, Baxter BK, Peters JW, Posewitz MC (2014) Evolutionary and biotechnological implications of robust hydrogenase activity in halophilic strains of tetraselmis. PLoS ONE. doi:10.1371/journal.pone.0085812
Diakonova AN, Khrushchev SS, Kovalenko IB, Riznichenko GY, Rubin AB (2016) Influence of pH and ionic strength on electrostatic properties of ferredoxin, FNR, and hydrogenase and the rate constants of their interaction. Phys Biol 13:056004. doi:10.1088/1478-3975/13/5/056004
Dubini A, Ghirardi ML (2015) Engineering photosynthetic organisms for the production of biohydrogen. Photosynth Res 123:241–253. doi:10.1007/s11120-014-9991-x
Eilenberg H, Weiner I, Ben-Zvi O, Pundak C, Marmari A, Liran O, Wecker MS, Milrad Y, Yacoby I (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. doi:10.1186/s13068-016-0601-3
Eroglu E, Melis A (2016) Microalgal hydrogen production research. Int J Hydrogen Energ 41:12772–12798. doi:10.1016/j.ijhydene.2016.05.115
Ewen KM, Ringle M, Bernhardt R (2012) Adrenodoxin: a versatile ferredoxin. IUBMB Life 64:506–512. doi:10.1002/iub.1029
Fukuyama K (2004) Structure and function of plant-type ferredoxins. Photosynth Res 81:289–301. doi:10.1023/B:PRES.0000036882.19322.0a
Guo Z, Li Y, Guo HY (2016) Characterization of H2 photoproduction by marine green alga Tetraselmis subcordiformis integrated with an alkaline fuel cell. Biotechnol Lett 38:435–440. doi:10.1007/s10529-015-2008-9
Hanke G, Mulo P (2013) Plant type ferredoxins and ferredoxin-dependent metabolism. Plant Cell Environ 36:1071–1084. doi:10.1111/pce.12046
Happe T, Naber JD (1993) Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. Eur J Biochem 214:475–481. doi:10.1111/j.1432-1033.1993.tb17944.x
Happe T, Mosler B, Naber JD (1994) Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii. Eur J Biochem 222:769–774. doi:10.1111/j.1432-1033.1994.tb18923.x
Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. BBA 1807:919–926. doi:10.1016/j.bbabio.2011.02.010
Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583:325–329. doi:10.1016/j.febslet.2008.12.018
Jiang WZ, Brueggeman AJ, Horken KM, Plucinak TM, Weeks DP (2014) Successful transient expression of Cas9 and single guide RNA genes in Chlamydomonas reinhardtii. Eukaryot Cell 13:1465–1469. doi:10.1128/ec.00213-14
Jinkerson RE, Jonikas MC (2015) Molecular techniques to interrogate and edit the Chlamydomonas nuclear genome. Plant J 82:393–412. doi:10.1111/tpj.12801
Lambertz C, Hemschemeier A, Happe T (2010) Anaerobic expression of the ferredoxin-encoding FDX5 gene of Chlamydomonas reinhardtii is regulated by the Crr1 transcription factor. Eukaryot Cell 9:1747–1754. doi:10.1128/EC.00127-10
Long H, Chang CH, King PW, Ghirardi ML, Kim K (2008) Brownian dynamics and molecular dynamics study of the association between hydrogenase and ferredoxin from Chlamydomonas reinhardtii. Biophys J 95:3753–3766. doi:10.1529/biophysj.107.127548
Meuser JE, D’Adamo S, Jinkerson RE, Mus F, Yang WQ, Ghirardi ML, Seibert M, Grossman AR, Posewitz MC (2012) Genetic disruption of both Chlamydomonas reinhardtii [FeFe]-hydrogenases: insight into the role of HYDA2 in H2 production. Biochem Biophys Res Commun 417:704–709. doi:10.1016/j.bbrc.2011.12.002
Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64:1063–1084. doi:10.1007/s00018-007-6477-4
Morales R, Chron MH, Hudry-Clergeon G, Petillot Y, Norager S, Medina M, Frey M (1999) Refined X-ray structures of the oxidized, at 1.3 angstrom, and reduced, at 1.17 angstrom, [2Fe-2S] ferredoxin from the cyanobacterium Anabaena PCC7119 show redox-linked conformational changes. BioChemistry 38:15764–15773. doi:10.1021/bi991578s
Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282:25475–25486. doi:10.1074/jbc.M701415200
Mussgnug JH (2015) Genetic tools and techniques for Chlamydomonas reinhardtii. Appl Microbiol Biotechnol 99:5407–5418. doi:10.1007/s00253-015-6698-7
Nei MaK S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York
Oey M, Sawyer AL, Ross IL, Hankamer B (2016) Challenges and opportunities for hydrogen production from microalgae. Plant Biotechnol J. doi:10.1111/pbi.12516
Okazaki K, Kabeya Y, Miyagishima SY (2010) The evolution of the regulatory mechanism of chloroplast division. Plant Signal Behav 5:164–167 pii]
Peden EA, Boehm M, Mulder DW, Davis R, Old WM, King PW, Ghirardi ML, Dubini A (2013) Identification of global ferredoxin interaction networks in Chlamydomonas reinhardtii. J Biol Chem 288:35192–35209. doi:10.1074/jbc.M113.483727
Pedroza-Garcia JA, Domenichini S, Bergounioux C, Benhamed M, Raynaud C (2016) Chloroplasts around the plant cell cycle. Curr Opin Plant Biol 34:107–113
Rodriguez-Ezpeleta N, Philippe H (2006) Plastid origin: replaying the tape. Curr Biol 16:R53–R56
Rumpel S, Siebel JF, Fares C, Duan J, Reijerse E, Happe T, Lubitz W, Winkler M (2014) Enhancing hydrogen production of microalgae by redirecting electrons from photosystem I to hydrogenase. Energy Environ Sci 7:3296–3301. doi:10.1039/c4ee01444h
Rumpel S, Siebel JF, Diallo M, Fares C, Reijerse EJ, Lubitz W (2015) Structural insight into the complex of ferredoxin and [FeFe] hydrogenase from Chlamydomonas reinhardtii. Chembiochem 16:1663–1669. doi:10.1002/cbic.201500130
Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum-evolution trees. Mol Biol Evol 9:945–967
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Scoma A, Krawietz D, Faraloni C, Giannelli L, Happe T, Torzillo G (2012) Sustained H2 production in a Chlamydomonas reinhardtii D1 protein mutant. J Biotechnol 157:613–619. doi:10.1016/j.jbiotec.2011.06.019
Shin M (2004) How is ferredoxin-NADP reductase involved in the NADP photoreduction of chloroplasts? Photosynth Res 80:307–313. doi:10.1023/B:PRES.0000030456.96329.f9
Shin SE, Lim JM, Koh HG, Kim EK, Kang NK, Jeon S, Kwon S, Shin WS, Lee B, Hwangbo K, Kim J, Ye SH, Yun JY, Seo H, Oh HM, Kim KJ, Kim JS, Jeong WJ, Chang YK, Jeong BR (2016) CRISPR/Cas9-induced knockout and knock-in mutations in Chlamydomonas reinhardtii. Sci Rep. doi:10.1038/srep27810
Suh J-Y, Tang C, Clore GM (2007) Role of electrostatic interactions in transient encounter complexes in protein-protein association investigated by paramagnetic relaxation enhancement. J Am Chem Soc 129:12954. doi:10.1021/ja0760978
Sybirna K, Bottin H (2013) New insights into the systems for heterologous synthesis and maturation of hydrogenases, the most efficient biohydrogen producers. Int J Hydrog Energ 38:13164–13171. doi:10.1016/j.ijhydene.2013.07.106
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Terauchi AM, Lu SF, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T, Merchant SS (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
Volgusheva A, Styring S, Mamedov F (2013) Increased photosystem II stability promotes H2 production in sulfur-deprived Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110:7223–7228. doi:10.1073/pnas.1220645110
Winkler M, Kuhlgert S, Hippler M, Happe T (2009) Characterization of the key step for light-driven hydrogen evolution in green algae. J Biol Chem 284:36620–36627. doi:10.1074/jbc.M109.053496
Winkler M, Hemschemeier A, Jacobs J, Stripp S, Happe T (2010) Multiple ferredoxin isoforms in Chlamydomonas reinhardtii: their role under stress conditions and biotechnological implications. Eur J Cell Biol 89:998–1004. doi:10.1016/j.ejcb.2010.06.018
Winkler M, Esselborn J, Happe T (2013) Molecular basis of [FeFe]-hydrogenase function an insight into the complex interplay between protein and catalytic cofactor. BBA 1827: 974–985. doi:10.1016/j.bbabio.2013.03.004
Yacoby I, Pochekailov S, Toporik H, Ghirardi ML, King PW, Zhang SG (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
Yang WQ, Wittkopp TM, Li XB, Warakanont J, Dubini A, Catalanotti C, Kim RG, Nowack ECM, Mackinder LCM, Aksoy M, Page MD, D’Adamo S, Saroussi S, Heinnickel M, Johnson X, Richaud P, Alric J, Boehm M, Jonikas MC, Benning C, Merchant SS, Posewitz MC, Grossman AR (2015) Critical role of Chlamydomonas reinhardtii ferredoxin-5 in maintaining membrane structure and dark metabolism. Proc Natl Acad Sci USA 112:14978–14983. doi:10.1073/pnas.1515240112
Acknowledgements
This research was supported by the Federal Ministry of Education and Research, Germany (ERASynBio consortium “Sun2Chem”) and the Volkswagen Foundation (LigH2t).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sawyer, A., Winkler, M. Evolution of Chlamydomonas reinhardtii ferredoxins and their interactions with [FeFe]-hydrogenases. Photosynth Res 134, 307–316 (2017). https://doi.org/10.1007/s11120-017-0409-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-017-0409-4