Abstract
The psbA gene family in cyanobacteria encodes different forms of the D1 protein that is part of the Photosystem II reaction centre. We have identified a phylogenetically distinct D1 group that is intermediate between previously identified G3-D1 and G4-D1 proteins (Cardona et al. Mol Biol Evol 32:1310–1328, 2015). This new group contained two subgroups: D1INT, which was frequently in the genomes of heterocystous cyanobacteria and D1FR that was part of the far-red light photoacclimation gene cluster of cyanobacteria. In addition, we have identified subgroups within G3, the micro-aerobically expressed D1 protein. There are amino acid changes associated with each of the subgroups that might affect the function of Photosystem II. We show a phylogenetically broad range of cyanobacteria have these D1 types, as well as the genes encoding the G2 protein and chlorophyll f synthase. We suggest identification of additional D1 isoforms and the presence of multiple D1 isoforms in phylogenetically diverse cyanobacteria supports the role of these proteins in conferring a selective advantage under specific conditions.
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References
Ago H, Adachi H, Umena Y, Tashiro T, Kawakami K, Kamiya N, Tian L, Han G, Kuang T, Liu Z, Wang F, Zou H, Enami I, Miyano M, Shen JR (2016) Novel features of eukaryotic Photosystem II revealed by its crystal structure analysis from a red alga. J Biol Chem 291:5676–5687. https://doi.org/10.1074/jbcM115.711689
Banerjee G, Ghosh I, Kim CJ, Debus RJ, Brudvig GW (2018) Substitution of the D1-Asn87 site in Photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach Photosystem II. J Biol Chem 293:2487–2497. https://doi.org/10.1074/jbc.M117.813170
Banerjee G, Ghosh I, Kim CJ, Debus RJ, Brudvig GW (2019) Bicarbonate rescues damaged proton-transfer pathway in Photosystem II. BBA Bioenerg 1860:611–617. https://doi.org/10.1016/j.bbabio.2019.06.014
Benson DA, Cavanaug M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2017) Genbank. Nucleic Acids Res 45:37–42. https://doi.org/10.1093/nar/gks1195
Bertoni M, Kiefer F, Biasini M, Bordoli L, Schwede T (2017) Modeling protein quaternary structure of homo- and hetero-oligomers beyond binary interactions by homology. Sci Rep 7:10480. https://doi.org/10.1038/s41598-017-09654-8
Bienert S, Waterhouse A, de Beer TAP, Tauriello G, Studer G, Bordoli L, Schwede T (2017) The SWISS-MODEL Repository - new features and functionality. Nucleic Acids Res 45:313–319. https://doi.org/10.1093/nar/gkw1132
Cardona T, Sedoud A, Cox N, Rutherford AW (2012) Charge separation in photosystem II: a comparative and evolutionary overview. BBA Bioenerg 1817:26–43. https://doi.org/10.1016/j.bbabio.2011.07.012
Cardona T, Murray JW, Rutherford AW (2015) Origin and evolution of water oxidation before the last common ancestor of the cyanobacteria. Mol Biol Evol 32:1310–1328. https://doi.org/10.1093/molbev/msv024
Cardona T, Sánchez‐Baracaldo P, Rutherford AW, Larkum AWD (2019) Early archean origin of photosystem II. Geobiology 17:127–150
Chen M, Schliep M, Willows RD, Cai ZL, Neilan BA, Scheer H (2010) A red-shifted chlorophyll. Science 329:1318–1319. https://doi.org/10.1126/science.1191127
Chen M, Li Y, Birch D, Willows RD (2012) A cyanobacterium that contains chlorophyll f – a red-absorbing photopigment. FEBS Lett 586:3249–3254. https://doi.org/10.1016/j.febslet.2012.06.045
Chen M, Hernandez-Prieto MA, Loughlin PC, Li Y, Willows RD (2019) Genome and proteome of the chlorophyll f-producing cyanobacterium Halomicronema hongdechloris: adaptative proteomic shifts under different light conditions. BMC Genomics 20:207. https://doi.org/10.1186/s12864-019-5587-3
Crawford TS, Hanning KR, Chua JP, Eaton-Rye JJ, Summerfield TC (2016) Comparison of D1′- and D1-containing PS II reaction centre complexes under different environmental conditions in Synechocystis sp. PCC 6803. Plant Cell Environ 39:1715–1726. https://doi.org/10.1111/pce.12738
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2 more models new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
DeLano WL (2002) Pymol: an open-source molecular graphics tool. CCP4 newsletter on protein. Crystallography 40:82–92
DeLano WL (2009) PyMOL molecular viewer Updates and refinements. In: Abstracts of Papers of the American Chemical Society (Vol. 238). American Chemical Society, Washington DC.
El Bissati K, Kirilovsky D (2001) Regulation of psbA and psaE expression by light quality in Synechocystis species PCC 6803. A redox control mechanism. Plant Physiol 125:1988–2000. https://doi.org/10.1104/pp.125.4.1988
Endo K, Kobayashi K, Wang H-T, Chu H-A, Shen J-R, Wada H (2019) Site-directed mutagenesis of two amino acid residues in cytochrome b559 α subunit that interact with a phosphatidylglycerol molecule (PG772) induces quinone-dependent inhibition of Photosystem II activity. Photosynth Res 139:267–279. https://doi.org/10.1007/s11120-018-0555-3
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838. https://doi.org/10.1126/science.1093087
Fletcher W, Yang Z (2010) The effect of insertions deletions and alignment errors on the branch-site test of positive selection. Mol Biol Evol 27:2257–2267. https://doi.org/10.1093/molbev/msq115
Funk C, Wiklund R, Schröder WP, Jansson C (2001) D1′ centers are less efficient than normal photosystem II centers. FEBS Lett 505:113–117. https://doi.org/10.1016/S0014-5793(01)02794-6
Gan F, Bryant DA (2015) Adaptive and acclimative responses of cyanobacteria to far-red light. Environ Microbiol 17:3450–3465. https://doi.org/10.1111/1462-2920.12992
Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA (2014) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–1317. https://doi.org/10.1126/science.1256963
Gan F, Shen G, Bryant DA (2015) Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life 5:4–24. https://doi.org/10.3390/life5010004
Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I (2012) The genome portal of the department of energy joint genome institute. Nucleic Acids Res 40:26–32. https://doi.org/10.1093/nar/gkt1069
Grim SL, Dick GJ (2016) Photosynthetic versatilityin the genome of Geitlerinema sp. PCC 9228 (Formerly Oscillatoria limnetica ‘Solar Lake’), a model anoxygenic photosynthetic cyanobacterium. Front Microbiol 7:26–32. https://doi.org/10.3389/fmicb.2016.01546
Guex N, Peitsch MC, Schwede T (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer A historical perspective. Electrophoresis 30:162–173. https://doi.org/10.1002/elps.200900140
Hakovirta JR, Prezioso S, Hodge D, Pillai SP, Weigel LM (2016) Identification and analysis of informative single nucleotide polymorphisms in 16S rRNA gene sequences of the Bacillus cereus group. J Clin Microbiol 54:2749–2756. https://doi.org/10.1128/JCM.01267-16
Hilton JA, Meeks JC, Zehr JP (2016) Surveying DNA Elements within functional genes of heterocyst-forming cyanobacteria. PLoS ONE 11:e0156034. https://doi.org/10.1371/journal.pone.0156034
Ho MY, Bryant DA (2019) Global transcriptional profiling of the cyanobacterium Chlorogloeopsis fritschii PCC 9212 in far-red light insights into the regulation of chlorophyll d synthesis. Front Microbiol 10:465. https://doi.org/10.3389/fmicb.2019.00465
Ho MY, Shen G, Canniffe DP, Zhao C, Bryant DA (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of Photosystem II. Science 353:aff9178. https://doi.org/10.1126/science.aaf9178
Ho MY, Niedzwiedzki DM, MacGregor-Chatwin C, Gerstenecker G, Hunter CN, Blankenship RE, Bryant DA (2019) Extensive remodeling of the photosynthetic apparatus alters energy transfer among photosynthetic complexes when cyanobacteria acclimate to far-red light. BBA Bioenerg. https://doi.org/10.1016/j.bbabio.2019.148064
Hongo JA, Castro GM, Cintra LC, Zerlotini A, Lobo FP (2015) POTION an end-to-end pipeline for positive Darwinian selection detection in genome-scale data through phylogenetic comparison of protein-coding genes. BMC Genomics 16:567. https://doi.org/10.1186/s12864-015-1765-0
Jaspers E, Overmann J (2004) Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70:4831–4839. https://doi.org/10.1128/AEM.70.8.4831-4839.2004
Kern J, Biesiadka J, Loll B, Saenger W, Zouni A (2007) Structure of the Mn4-Ca cluster as derived from X-ray diffraction. Photosynth Res 92:389–405. https://doi.org/10.1007/s11120-007-9173-1
Kern J, Chatterjee R, Young ID et al (2018) Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature 563:421–425. https://doi.org/10.1038/s41586-018-0681-2
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320. https://doi.org/10.1093/molbev/msn067
Li B, Lopes JS, Foster PG, Embley TM, Cox CJ (2014) Compositional biases among synonymous substitutions cause conflict between gene and protein trees for plastid origins. Mol Biol Evol 31:1697–1709. https://doi.org/10.1093/molbev/msu105
Mares J, Johansen JR, Hauer T, Zima J Jr, Ventura S, Cuzman O, Tiribilli B, Kastovsky J (2019) Taxonomic resolution of the genus Cyanothece (Chroococcales, Cyanobacteria), with a treatment on Gloeothece and three new genera, Crocosphaera, Rippkaea, and Zehria. J Phycol 55:578–610. https://doi.org/10.1111/jpy.12853
Masuda T, Bernát G, Bečková M, Kotabová E, Lawrenz E, Lukeš M, Komenda J, Prášil O (2018) Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ Microbiol 20:546–560. https://doi.org/10.1111/1462-2920.13963
Mella-Flores D, Six C, Ratin M, Partensky F, Boutte C, Le Corguillé G, Blot N, Gourvil P, Kolowrat C, Garczarek L, Marie D (2012) Prochlorococcus and Synechococcus have evolved different adaptive mechanisms to cope with light and UV stress. Front Microbiol 3:285. https://doi.org/10.3389/fmicb.2012.00285
Moore KR, Magnabosco C, Momper L, Gold DA, Bosak T, Fournier GP (2019) An expanded ribosomal phylogeny of cyanobacteria supports a deep placement of plastids. Front Microbiol 10:1612. https://doi.org/10.3389/fmicb.2019.01612
Mulo P, Sicora C, Aro EM (2009) Cyanobacterial psbA gene family optimization of oxygenic photosynthesis. Cell Mol Life Sci 66:3697. https://doi.org/10.1007/s00018-009-0103-6
Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria green algae and higher plants from transcription to PSII repair. BBA Bioenerg 1817:247–257. https://doi.org/10.1016/j.bbabio.2011.04.011
Murray JW (2012) Sequence variation at the oxygen-evolving centre of Photosystem II a new class of ‘rogue’ cyanobacterial D1 proteins. Photosynth Res 110:177–184. https://doi.org/10.1007/s11120-011-9714-5
Narusaka Y, Murakami A, Saeki M, Kobayashi H, Satoh K (1996) Preliminary characterization of a photo-tolerant mutant of Synechocystis sp. PCC 6803 obtained by in vitro random mutagenesis of psbA2. Plant Sci 115:261–266. https://doi.org/10.1016/0168-9452(96)04393-2
Narusaka Y, Narusaka M, Satoh K, Kobayashi H (1999) In vitro random mutagenesis of the D1 protein of the Photosystem II reaction center confers phototolerance on the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 274:23270–23275. https://doi.org/10.1074/jbc.274.33.23270
Nordberg H, Cantor M, Dusheyko S, Hua S, Polakov A, Shabalov I, Smirnova T, Grigorie IV, Dubchak I (2014) The genome portal of the department of energy joint genome institute 2014 updates. Nucleic Acids Res 42:26–31. https://doi.org/10.1093/nar/gkt1069
Nürnberg DJ, Morton J, Santabarbara S, Telfer A, Joliot P, Antonaru LA, Ruban AV, Cardona T, Krausz E, Boussac A, Fantuzzi A, Rutherford AW (2018) Photochemistry beyond the red limit in chlorophyll f–containing photosystems. Science 360:1210–1213. https://doi.org/10.1126/science.aar8313
Ohkubo S, Miyashita H (2017) A niche for cyanobacteria producing chlorophyll f within a microbial mat. ISME J 11:2368–2378. https://doi.org/10.1038/ismej.2017.98
Park J-J, Lechno-Yossef S, Wolk CP, Vieille C (2013) Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically. BMC Genomics 14:759. https://doi.org/10.1186/1471-2164-14-759
Partensky F, Six C, Ratin M, Garczarek L, Vaulot D, Probert I, Calteau A, Gourvil P, Marie D, Grébert T, Bouchier C (2018) A novel species of the marine cyanobacterium Acaryochloris with a unique pigment content and lifestyle. Sci Rep 8:9142. https://doi.org/10.1038/s41598-018-27542-7
Ponce-Toledo RI, Deschamps P, López-García P, Zivanovic Y, Benzerara K, David MD (2017) An Early-Branching Freshwater Cyanobacterium at the origin of plastids. Curr Biol 27:386–391. https://doi.org/10.1016/j.cub.2016.11.056
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project improved data processing and web-based tools. Nucleic Acids Res 41:590–596. https://doi.org/10.1093/nar/gks1219
Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424:1042. https://doi.org/10.1038/nature01947
Sánchez-Baracaldo P, Raven JA, Pisani D, Knoll AH (2017) Early photosynthetic eukaryotes inhabited low-salinity habitats. Proc Natl Acad Sci USA 114:7737–7745. https://doi.org/10.1073/pnas.1620089114
Saw JH, Schatz M, Brown MV, Kunkel DD, Foster JS, Shick H, Christensen S, Hou S, Wan X, Donachie SP (2013) Cultivation and complete genome sequencing of Gloeobacter kilaueensis sp nov, from a lava cave in Kīlauea Caldera Hawai'i. PLoS ONE 8:e76376. https://doi.org/10.1371/journal.pone.0076376
Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, Hagemann M, Paulsen I, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol R 73:249–299. https://doi.org/10.1128/MMBR.00035-08
Shen J-R (2015) The structure of Photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol 66:23–48. https://doi.org/10.1146/annurev-arplant-050312-120129
Shen G, Canniffe DP, Ho MY, Kurashov V, van der Est A, Golbeck JH, Bryant DA (2019) Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002. Photosynth Res 140:1–16. https://doi.org/10.1007/s11120-018-00610-9
Shih PM, Wu D, Latifi A, Axen SD, Fewer DP, Talla E, Calteau A, Cai F, De Marsac NT, Rippka R, Herdman M (2013) Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc Natl Acad Sci USA 110:1053–1058. https://doi.org/10.1073/pnas.1217107110
Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116. https://doi.org/10.1093/oxfordjournals.molbev.a026201
Shindyalov IN, Bourne PE (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Prot Eng 11:739–747. https://doi.org/10.1093/protein/11.9.739
Sicora C, Wiklund R, Jansson C, Vass I (2004) Charge stabilization and recombination in photosystem II containing the D1′ protein product of the psbAI gene in Synechocystis 6803. Phys Chem Chem Phys 6:4832–4837
Sicora C, Ho FM, Salminen T, Styring S, Aro EM (2009) Transcription of a “silent” cyanobacterial psbA gene is induced by microaerobic conditions. BBA Bioenerg 1787:105–112. https://doi.org/10.1016/j.bbabio.2008.12.002
Sicora CI, Chiș I, Chiș C, Sicora O (2019) Regulation of PSII function in Cyanothece sp. ATCC 51142 during a light–dark cycle. Photosynth Res 139:461–473. https://doi.org/10.1007/s11120-018-0598-5
Stamatakis A (2006) RAxML-VI-HPC maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, Yamashita K, Yamamoto M, Ago H, Shen JR (2015) Native structure of Photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature 517:99–103. https://doi.org/10.1038/nature13991
Suga M, Akita F, Sugahara M et al (2017) Light-induced structural changes and the site of O=O bond formation in PS II caught by XFEL. Nature 543:131–135. https://doi.org/10.1038/nature21400
Sugiura M, Ozaki Y, Nakamura M, Cox N, Rappaport F, Boussac A (2014) The D1–173 amino acid is a structural determinant of the critical interaction between D1-Tyr161 (TyrZ) and D1-His190 in Photosystem II. BBA Bioenerg 1837:1922–1931. https://doi.org/10.1016/j.bbabio.2014.08.008
Summerfield TC, Toepel J, Sherman LA (2008) Low-oxygen induction of normally cryptic psbA genes in cyanobacteria. Biochemistry 47:12939–12941. https://doi.org/10.1021/bi8018916
Swofford DL (2001) Paup*: Phylogenetic analysis using parsimony (and other methods) 4.0. B5.
Toepel J, Welsh E, Summerfield TC, Pakrasi HB, Sherman LA (2008) Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. J Bacteriol 190:3904–3913. https://doi.org/10.1128/JB.00206-08
Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving Photosystem II at a resolution of 1.9 Å. Nature 473:55–60. https://doi.org/10.1038/nature09913
Vinyard DJ, Brudvig GW (2018) Progress toward a molecular mechanism of water oxidation in Photosystem II. Annu Rev Phys Chem 68:101–116. https://doi.org/10.1146/annurev-physchem-052516-044820
Vinyard DJ, Gimpel J, Ananyev GM, Mayfield SP, Dismukes GC (2014) Engineered Photosystem II reaction centers optimize photochemistry versus photoprotection at different solar intensities. J Am Chem Soc 136:4048–4055. https://doi.org/10.1021/ja5002967
Wada H, Murata N (2007) The essential role of phosphatidylglycerol in photosynthesis. Photosynth Res 92:205–215. https://doi.org/10.1007/s11120-007-9203-z
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:296–303. https://doi.org/10.1093/nar/gky427
Wegener KM, Nagarajan A, Pakrasi HB (2015) An atypical psbA gene encodes a sentinel D1 protein to form a physiologically relevant inactive Photosystem II complex in cyanobacteria. J Biol Chem 290:3764–3774. https://doi.org/10.1074/jbc.M114.604124
Wei X, Su X, Cao P et al (2016) Structure of spinach Photosystem II – LHCII supercomplex at 3.2 Å resolution. Nature 534:69–74
Wiklund R, Salih GF, Mäenpää P, Jansson C (2001) Engineering of the protein environment around the redox-active TyrZ in Photosystem II. The role of F186 and P162 in the D1 protein of Synechocystis 6803. Eur J Biochem 268:5356–5364. https://doi.org/10.1046/j.0014-2956.2001.02466.x
Xu B, Yang Z (2013) PAMLX a graphical user interface for PAML. Mol Biol Evol 30:2723–2724. https://doi.org/10.1093/molbev/mst179
Yamasato A, Kamada T, Satoh K (2002) Random mutagenesis targeted to the psbAII gene of Synechocystis sp. PCC 6803 to identify functionally important residues in the D1 protein of the Photosystem II reaction center. Plant Cell Physiol 43:540–548. https://doi.org/10.1093/pcp/pcf066
Yang Z (2007) PAML 4 phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. https://doi.org/10.1093/molbev/msm088
Zabelin AA, Shkuropatova VA, Makhneva ZK, Moskalenko AA, Shuvalov VA, Shkuropatov AY (2014) Chemically modified reaction centers of Photosystem II: Exchange of pheophytin a with 7-deformyl-7-hydroxymethyl-pheophytin b. BBA Bioenerg 1837:1870–1881. https://doi.org/10.1016/j.bbabio.2014.08.004
Acknowledgements
The authors would like to acknowledge Andy Nilsen for the valuable discussions while creating the phylogenetic trees and Bronwyn Carlisle for helping to finalise the figures for publication. KJS is supported by a University of Otago Division of Sciences PhD Scholarship. Additional funding was provided by a University of Otago research grant to TCS.
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Sheridan, K.J., Duncan, E.J., Eaton-Rye, J.J. et al. The diversity and distribution of D1 proteins in cyanobacteria. Photosynth Res 145, 111–128 (2020). https://doi.org/10.1007/s11120-020-00762-7
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DOI: https://doi.org/10.1007/s11120-020-00762-7