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Isolation and characterization of trimeric and monomeric PSI cores from Acaryochloris marina MBIC11017

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Abstract

Photosystem I (PSI) catalyzes light-induced electron-transfer reactions and has been observed to exhibit various oligomeric states and different energy levels of chlorophylls (Chls) in response to oligomerization. However, the biochemical and spectroscopic properties of a PSI monomer containing Chls d are not well understood. In this study, we successfully isolated and characterized PSI monomers from the cyanobacterium Acaryochloris marina MBIC11017, and compared their properties with those of the A. marina PSI trimer. The PSI trimers and monomers were prepared using trehalose density gradient centrifugation after anion-exchange and hydrophobic interaction chromatography. The polypeptide composition of the PSI monomer was found to be consistent with that of the PSI trimer. The absorption spectrum of the PSI monomer showed the Qy band of Chl d at 704 nm, which was blue-shifted from the peak at 707 nm observed in the PSI-trimer spectrum. The fluorescence-emission spectrum of the PSI monomer measured at 77 K exhibited a peak at 730 nm without a broad shoulder in the range of 745–780 nm, which was clearly observed in the PSI-trimer spectrum. These spectroscopic properties of the A. marina PSI trimer and monomer suggest different formations of low-energy Chls d between the two types of PSI cores. Based on these findings, we discuss the location of low-energy Chls d in A. marina PSIs.

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All data supporting the findings of this study are available within the paper and its Supplementary Information.

Change history

  • 26 May 2023

    The Abbreviations were corrected from ‘Car Catrenoid’ to ‘Car Carotenoid’.

Abbreviations

β-DDM:

n-Dodecyl-β-D-maltoside

Car:

Carotenoid

Chl:

Chlorophyll

PPFD:

Photosynthetic photon flux density

PS:

Photosystem

References

  • Brettel K, Leibl W (2001) Electron transfer in photosystem I. Biochim Biophys Acta, Bioenerg 1507:100–114

    Article  CAS  Google Scholar 

  • Çoruh O, Frank A, Tanaka H, Kawamoto A, El-Mohsnawy E, Kato T, Namba K, Gerle C, Nowaczyk MM, Kurisu G (2021) Cryo-EM structure of a functional monomeric Photosystem I from Thermosynechococcus elongatus reveals red chlorophyll cluster. Commun Biol 4:304

    Article  PubMed Central  PubMed  Google Scholar 

  • El-Mohsnawy E, Kopczak MJ, Schlodder E, Nowaczyk M, Meyer HE, Warscheid B, Karapetyan NV, Rögner M (2010) Structure and function of intact photosystem 1 monomers from the cyanobacterium Thermosynechococcus elongatus. Biochemistry 49:4740–4751

    Article  CAS  PubMed  Google Scholar 

  • Fromme P, Jordan P, Krauß N (2001) Structure of photosystem I. Biochim Biophys Acta, Bioenerg 1507:5–31

    Article  CAS  Google Scholar 

  • Gobets B, van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta, Bioenerg 1507:80–99

    Article  CAS  Google Scholar 

  • Golbeck JH (1992) Structure and function of photosystem I. Ann Rev Plant Physiol Plant Mol Biol 43:293–324

    Article  CAS  Google Scholar 

  • Hamaguchi T, Kawakami K, Shinzawa-Itoh K, Inoue-Kashino N, Itoh S, Ifuku K, Yamashita E, Maeda K, Yonekura K, Kashino Y (2021) Structure of the far-red light utilizing photosystem I of Acaryochloris marina. Nat Commun 12:2333

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hippler M, Nelson N (2021) The plasticity of photosystem I. Plant Cell Physiol 62:1073–1081

    Article  CAS  PubMed  Google Scholar 

  • Hu Q, Miyashita H, Iwasaki I, Kurano N, Miyachi S, Iwaki M, Itoh S (1998) A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc Natl Acad Sci USA 95:13319–13323

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ikeuchi M, Inoue Y (1988) A new photosystem II reaction center component (4.8 kDa protein) encoded by chloroplast genome. FEBS Lett 241:99–104

    Article  CAS  PubMed  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411:909–917

    Article  CAS  PubMed  Google Scholar 

  • Karapetyan NV, Schlodder E, van Grondelle R, Dekker JP (2006) The long wavelength chlorophylls of Photosystem I. In: Golbeck JH (ed) Photosystem I: the Light-Driven Plastocyanin: Ferredoxin Oxidoreductase. Springer, Dordrecht, The Netherlands, pp 177–192

    Chapter  Google Scholar 

  • Kato K, Nagao R, Jiang T-Y, Ueno Y, Yokono M, Chan SK, Watanabe M, Ikeuchi M, Shen J-R, Akimoto S, Miyazaki N, Akita F (2019) Structure of a cyanobacterial photosystem I tetramer revealed by cryo-electron microscopy. Nat Commun 10:4929

    Article  PubMed Central  PubMed  Google Scholar 

  • Kato K, Hamaguchi T, Nagao R, Kawakami K, Ueno Y, Suzuki T, Uchida H, Murakami A, Nakajima Y, Yokono M, Akimoto S, Dohmae N, Yonekura K, Shen J-R (2022a) Structural basis for the absence of low-energy chlorophylls in a photosystem I trimer from Gloeobacter violaceus. eLife 11:e73990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kato K, Nagao R, Ueno Y, Yokono M, Suzuki T, Jiang T-Y, Dohmae N, Akita F, Akimoto S, Miyazaki N, Shen J-R (2022b) Structure of a tetrameric photosystem I from a glaucophyte alga Cyanophora paradoxa. Nat Commun 13:1679

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kimura A, Kitoh-Nishioka H, Aota T, Hamaguchi T, Yonekura K, Kawakami K, Shinzawa-Itoh K, Inoue-Kashino N, Ifuku K, Yamashita E, Kashino Y, Itoh S (2022) Theoretical model of the far-red-light-adapted photosystem I reaction center of cyanobacterium Acaryochloris marina using chlorophyll d and the effect of chlorophyll exchange. J Phys Chem B 126:4009–4021

    Article  CAS  PubMed  Google Scholar 

  • Kühl M, Chen M, Ralph PJ, Schreiber U, Larkum AWD (2005) A niche for cyanobacteria containing chlorophyll d. Nature 433:820

    Article  PubMed  Google Scholar 

  • Li M, Calteau A, Semchonok DA, Witt TA, Nguyen JT, Sassoon N, Boekema EJ, Whitelegge J, Gugger M, Bruce BD (2019) Physiological and evolutionary implications of tetrameric photosystem I in cyanobacteria. Nat Plants 5:1309–1319

    Article  CAS  PubMed  Google Scholar 

  • Miller SR, Augustine S, Olson TL, Blankenship RE, Selker J, Wood AM (2005) Discovery of a free-living chlorophyll d-producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene. Proc Natl Acad Sci USA 102:850–855

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miyashita H, Ikemoto H, Kurano N, Adachi K, Chihara M, Miyachi S (1996) Chlorophyll d as a major pigment. Nature 383:402–402

    Article  CAS  Google Scholar 

  • Murakami A, Miyashita H, Iseki M, Adachi K, Mimuro M (2004) Chlorophyll d in an epiphytic cyanobacterium of red algae. Science 303:1633

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Ishii A, Tada O, Suzuki T, Dohmae N, Okumura A, Iwai M, Takahashi T, Kashino Y, Enami I (2007) Isolation and characterization of oxygen-evolving thylakoid membranes and Photosystem II particles from a marine diatom Chaetoceros gracilis. Biochim Biophys Acta, Bioenerg 1767:1353–1362

    Article  CAS  Google Scholar 

  • Nagao R, Yamaguchi M, Nakamura S, Ueoka-Nakanishi H, Noguchi T (2017) Genetically introduced hydrogen bond interactions reveal an asymmetric charge distribution on the radical cation of the special-pair chlorophyll P680. J Biol Chem 292:7474–7486

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nagao R, Ueno Y, Akimoto S, Shen J-R (2020a) Effects of CO2 and temperature on photosynthetic performance in the diatom Chaetoceros gracilis. Photosynth Res 146:189–195

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Ueno Y, Jiang T-Y, Shen J-R, Akimoto S (2020b) pH-induced regulation of excitation energy transfer in the cyanobacterial photosystem I tetramer. J Phys Chem B 124:1949–1954

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Ueno Y, Shen J-R, Akimoto S (2020c) Excitation-energy transfer and quenching in diatom PSI-FCPI upon P700 cation formation. J Phys Chem B 124:1481–1486

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Kato K-H, Ueno Y, Shen J-R, Akimoto S (2021) High-light modification of excitation-energy-relaxation processes in the green flagellate Euglena gracilis. Photosynth Res 149:303–311

    Article  CAS  PubMed  Google Scholar 

  • Nagao R (2022) Handbook of cyanobacterial PSI structures. [Kindle edition]. Retrieved from Amazon.com. https://www.amazon.co.jp/Handbook-Cyanobacterial-PSI-Structures-English-ebook/dp/B09Z8R7B4K,

  • Naschberger A, Fadeeva M, Klaiman D, Borovikova-Sheinker A, Caspy I, Nelson N, Amunts A (2022a) Structure of plant Photosystem I in a native assembly state. Research Square. https://doi.org/10.21203/rs.3.rs-2406494/v1

    Article  Google Scholar 

  • Naschberger A, Mosebach L, Tobiasson V, Kuhlgert S, Scholz M, Perez-Boerema A, Ho TTH, Vidal-Meireles A, Takahashi Y, Hippler M, Amunts A (2022b) Algal photosystem I dimer and high-resolution model of PSI-plastocyanin complex. Nat Plants 8:1191–1201

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nelson N, Junge W (2015) Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu Rev Biochem 84:659–683

    Article  CAS  PubMed  Google Scholar 

  • Schägger H, von Jagow G (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199:223–231

    Article  PubMed  Google Scholar 

  • Schlodder E, Çetin M, Byrdin M, Terekhova IV, Karapetyan NV (2005) P700+-and 3P700-induced quenching of the fluorescence at 760 nm in trimeric Photosystem I complexes from the cyanobacterium Arthrospira platensis. Biochim Biophys Acta, Bioenerg 1706:53–67

    Article  CAS  Google Scholar 

  • Schlodder E, Shubin VV, El-Mohsnawy E, Roegner M, Karapetyan NV (2007) Steady-state and transient polarized absorption spectroscopy of photosystem I complexes from the cyanobacteria Arthrospira platensis and Thermosynechococcus elongatus. Biochim Biophys Acta, Bioenerg 1767:732–741

    Article  CAS  Google Scholar 

  • Schlodder E, Hussels M, Çetin M, Karapetyan NV, Brecht M (2011) Fluorescence of the various red antenna states in photosystem I complexes from cyanobacteria is affected differently by the redox state of P700. Biochim Biophys Acta, Bioenerg 1807:1423–1431

    Article  CAS  Google Scholar 

  • Shen J-R (2022) Structure, function, and variations of the photosystem I-antenna supercomplex from different photosynthetic organisms. In: Harris JR, Marles-Wright J (eds) Macromolecular Protein Complexes IV. Subcellular Biochemistry, vol 99. Springer, Cham., pp 351–377

    Chapter  Google Scholar 

  • Shibata Y, Yamagishi A, Kawamoto S, Noji T, Itoh S (2010) Kinetically distinct three red chlorophylls in photosystem I of Thermosynechococcus elongatus revealed by femtosecond time-resolved fluorescence spectroscopy at 15 K. J Phys Chem B 114:2954–2963

    Article  CAS  PubMed  Google Scholar 

  • Shubin VV, Bezsmertnaya IN, Karapetyan NV (1995) Efficient energy transfer from the long-wavelength antenna chlorophylls to P700 in photosystem I complexes from Spirulina platensis. J Photochem Photobiol B 30:153–160

    Article  CAS  Google Scholar 

  • Sivakumar V, Wang R, Hastings G (2003) Photo-oxidation of P740, the primary electron donor in photosystem I from Acaryochloris marina. Biophys J 85:3162–3172

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Swingley WD, Chen M, Cheung PC, Conrad AL, Dejesa LC, Hao J, Honchak BM, Karbach LE, Kurdoglu A, Lahiri S, Mastrian SD, Miyashita H, Page L, Ramakrishna P, Satoh S, Sattley WM, Shimada Y, Taylor HL, Tomo T, Tsuchiya T, Wang ZT, Raymond J, Mimuro M, Blankenship RE, Touchman JW (2008) Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proc Natl Acad Sci USA 105:2005–2010

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Taniguchi M, Lindsey JS (2021) Absorption and fluorescence spectral database of chlorophylls and analogues. Photochem Photobiol 97:136–165

    Article  CAS  PubMed  Google Scholar 

  • Tomo T, Suzuki T, Hirano E, Tsuchiya T, Miyashita H, Dohmae N, Mimuro M (2006) Reversible absorption change of chlorophyll d in solutions. Chem Phys Lett 423:282–287

    Article  CAS  Google Scholar 

  • Tomo T, Kato Y, Suzuki T, Akimoto S, Okubo T, Noguchi T, Hasegawa K, Tsuchiya T, Tanaka K, Fukuya M, Dohmae N, Watanabe T, Mimuro M (2008) Characterization of highly purified photosystem I complexes from the chlorophyll d-dominated cyanobacterium Acaryochloris marina MBIC 11017. J Biol Chem 283:18198–18209

    Article  CAS  PubMed  Google Scholar 

  • Turconi S, Kruip J, Schweitzer G, Rögner M, Holzwarth AR (1996) A comparative fluorescence kinetics study of Photosystem I monomers and trimers from Synechocystis PCC 6803. Photosynth Res 49:263–268

    Article  CAS  PubMed  Google Scholar 

  • Ulrich NJ, Uchida H, Kanesaki Y, Hirose E, Murakami A, Miller SR (2021) Reacquisition of light-harvesting genes in a marine cyanobacterium confers a broader solar niche. Curr Biol 31:1539–1546

    Google Scholar 

  • van Grondelle R, Dekker JP, Gillbro T, Sundstrom V (1994) Energy transfer and trapping in photosynthesis. Biochim Biophys Acta, Bioenerg 1187:1–65

    Article  CAS  Google Scholar 

  • Watanabe M, Kubota H, Wada H, Narikawa R, Ikeuchi M (2011) Novel supercomplex organization of photosystem I in Anabaena and Cyanophora paradoxa. Plant Cell Physiol 52:162–168

    Article  CAS  PubMed  Google Scholar 

  • Xu C, Zhu Q, Chen J-H, Shen L, Yi X, Huang Z, Wang W, Chen M, Kuang T, Shen J-R, Zhang X, Han G (2021) A unique photosystem I reaction center from a chlorophyll d-containing cyanobacterium Acaryochloris marina. J Integr Plant Biol 63:1740–1752

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto H, Uesaka K, Tsuzuki Y, Yamakawa H, Itoh S, Fujita Y (2022) Comparative genomic analysis of the marine cyanobacterium Acaryochloris marina MBIC10699 reveals the impact of phycobiliprotein reacquisition and the diversity of Acaryochloris plasmids. Microorganisms 10:1374.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zapata M, Rodríguez F, Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195:29–45

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Ms. Kumiyo Kato and Ms. Satoko Kakiuchi for her assistance in this study. This work was supported by JSPS KAKENHI grant Nos. JP21K19085 (R.N.), JP20H02914 (K.K.), JP21K06101 (T.T.), and JP22H04916 (J.-R.S.).

Funding

Japan Society for the Promotion of Science, JP21K19085, JP20H02914, JP21K06101, JP22H04916

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Authors and Affiliations

  1. Faculty of Agriculture, Shizuoka University, Shizuoka, 422-8529, Japan

    Ryo Nagao

  2. Research Institute for Interdisciplinary Science and Graduate School of Natural Science and Technology, Okayama University, Okayama, 700-8530, Japan

    Haruya Ogawa, Naoki Tsuboshita, Koji Kato & Jian-Ren Shen

  3. Department of Physics, Graduate School of Science, Tokyo University of Science, Tokyo, 162-8601, Japan

    Reona Toyofuku & Tatsuya Tomo

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  1. Ryo Nagao
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  2. Haruya Ogawa
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  3. Naoki Tsuboshita
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  4. Koji Kato
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Contributions

R.N. conceived the project; R.T. and T.T. provided the cells; R.N. prepared the trimeric and monomeric PSI cores; R.N., H.O., and N.T. analyzed their biochemical and spectroscopic properties; R.N., K.K., T.T., and J.-R.S. provided experimental and funding resorces; R.N. wrote the manuscript, and all of the authors joined the discussion of the results.

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Correspondence to Ryo Nagao.

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Nagao, R., Ogawa, H., Tsuboshita, N. et al. Isolation and characterization of trimeric and monomeric PSI cores from Acaryochloris marina MBIC11017. Photosynth Res 157, 55–63 (2023). https://doi.org/10.1007/s11120-023-01025-x

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