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Biochemical and spectroscopic characterization of PSI-LHCI from the red alga Cyanidium caldarium

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Abstract

Light-harvesting complexes (LHCs) have been diversified in oxygenic photosynthetic organisms, and play an essential role in capturing light energy which is transferred to two types of photosystem cores to promote charge-separation reactions. Red algae are one of the groups of photosynthetic eukaryotes, and their chlorophyll (Chl) a-binding LHCs are specifically associated with photosystem I (PSI). In this study, we purified three types of preparations, PSI-LHCI supercomplexes, PSI cores, and isolated LHCIs, from the red alga Cyanidium caldarium, and examined their properties. The polypeptide bands of PSI-LHCI showed characteristic PSI and LHCI components without contamination by other proteins. The carotenoid composition of LHCI displayed zeaxanthins, β-cryptoxanthins, and β-carotenes. Among the carotenoids, zeaxanthins were enriched in LHCI. On the contrary, both zeaxanthins and β-cryptoxanthins could not be detected from PSI, suggesting that zeaxanthins and β-cryptoxanthins are bound to LHCI but not PSI. A Qy peak of Chl a in the absorption spectrum of LHCI was shifted to a shorter wavelength than those in PSI and PSI-LHCI. This tendency is in line with the result of fluorescence-emission spectra, in which the emission maxima of PSI-LHCI, PSI, and LHCI appeared at 727, 719, and 677 nm, respectively. Time-resolved fluorescence spectra of LHCI represented no 719 and 727-nm fluorescence bands from picoseconds to nanoseconds. These results indicate that energy levels of Chls around/within LHCIs and within PSI are changed by binding LHCIs to PSI. Based on these findings, we discuss the expression, function, and structure of red algal PSI-LHCI supercomplexes.

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Abbreviations

β-DDM:

n-Dodecyl-β-d-maltoside

Chl:

Chlorophyll

LHC:

Light-harvesting complex

LHCI:

LHC specific to PSI

PS:

Photosystem

TRF:

Time-resolved fluorescence

References

  • Abram M, Białek R, Szewczyk S, Karolczak J, Gibasiewicz K, Kargul J (2020) Remodeling of excitation energy transfer in extremophilic red algal PSI-LHCI complex during light adaptation. Biochim Biophys Acta, Bioenerg 1861:148093

    Article  CAS  PubMed  Google Scholar 

  • Akimoto S, Yokono M, Ohmae M, Yamazaki I, Tanaka A, Higuchi M, Tsuchiya T, Miyashita H, Mimuro M (2005) Ultrafast excitation relaxation dynamics of lutein in solution and in the light-harvesting complexes II isolated from Arabidopsis thaliana. J Phys Chem B 109:12612–12619

    Article  CAS  PubMed  Google Scholar 

  • Akimoto S, Yokono M, Hamada F, Teshigahara A, Aikawa S, Kondo A (2012) Adaptation of light-harvesting systems of Arthrospira platensis to light conditions, probed by time-resolved fluorescence spectroscopy. Biochim Biophys Acta, Bioenerg 1817:1483–1489

    Article  CAS  Google Scholar 

  • Akimoto S, Teshigahara A, Yokono M, Mimuro M, Nagao R, Tomo T (2014) Excitation relaxation dynamics and energy transfer in fucoxanthin-chlorophyll a/c-protein complexes, probed by time-resolved fluorescence. Biochim Biophys Acta, Bioenerg 1837:1514–1521

    Article  CAS  Google Scholar 

  • Allen MB (1959) Studies with Cyanidium caldarium, an anomalously pigmented chlorophyte. Arch Mikrobiol 32:270–277

    Article  CAS  PubMed  Google Scholar 

  • Antoshvili M, Caspy I, Hippler M, Nelson N (2019) Structure and function of photosystem I in Cyanidioschyzon merolae. Photosynth Res 139:499–508

    Article  CAS  PubMed  Google Scholar 

  • Blankenship RE (2021) Molecular mechanisms of photosynthesis, 3rd edn. Wiley, Blackwell, Oxford, UK

    Google Scholar 

  • Breithaupt DE, Bamedi A (2001) Carotenoid esters in vegetables and fruits: a screening with emphasis on β-cryptoxanthin esters. J Agric Food Chem 49:2064–2070

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Busch A, Nield J, Hippler M (2010) The composition and structure of photosystem I-associated antenna from Cyanidioschyzon merolae. Plant J 62:886–897

    Article  CAS  PubMed  Google Scholar 

  • Chen JP, Tai CY, Chen BH (2004) Improved liquid chromatographic method for determination of carotenoids in Taiwanese mango (Mangifera indica L.). J Chromatogr A 1054:261–268

    Article  CAS  PubMed  Google Scholar 

  • Croce R, van Amerongen H (2013) Light-harvesting in photosystem I. Photosynth Res 116:153–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    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 

  • Gardian Z, Bumba L, Schrofel A, Herbstova M, Nebesarova J, Vacha F (2007) Organisation of photosystem I and photosystem II in red alga Cyanidium caldarium: encounter of cyanobacterial and higher plant concepts. Biochim Biophys Acta, Bioenerg 1767:725–731

    Article  CAS  Google Scholar 

  • Giera W, Szewczyk S, McConnell MD, Redding KE, van Grondelle R, Gibasiewicz K (2018) Uphill energy transfer in photosystem I from Chlamydomonas reinhardtii. Time-resolved fluorescence measurements at 77 K. Photosynth Res 137:321–335

    Article  CAS  PubMed  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 

  • Hamada F, Murakami A, Akimoto S (2017) Adaptation of divinyl chlorophyll a/b-containing cyanobacterium to different light conditions: three strains of Prochlorococcus marinus. J Phys Chem B 121:9081–9090

    Article  CAS  PubMed  Google Scholar 

  • Haniewicz P, Abram M, Nosek L, Kirkpatrick J, El-Mohsnawy E, Janna Olmos JD, Kouŕil R, Kargul JM (2018) Molecular mechanisms of photoadaptation of photosystem I supercomplex of in an evolutionary cyanobacterial/algal intermediate. Plant Physiol 176:1433–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haworth P, Watson JL, Arntzen CJ (1983) The detection, isolation and characterization of a light-harvesting complex which is specifically associated with photosystem I. Biochim Biophys Acta, Bioenerg 724:151–158

    Article  CAS  Google Scholar 

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

    Article  CAS  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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S-L, Chiang Y-R, Yoon HS, Fu H-Y (2020) Comparative genome analysis reveals Cyanidiococcus gen. nov., a new extremophilic red algal genus sister to Cyanidioschyzon (Cyanidioschyzonaceae, Rhodophyta). J Phycol 56:1428–1442

    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

  • Nagao R, Yokono M, Akimoto S, Tomo T (2013) High excitation energy quenching in fucoxanthin chlorophyll a/c-binding protein complexes from the diatom Chaetoceros gracilis. J Phys Chem B 117:6888–6895

    Article  CAS  PubMed  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  PubMed Central  Google Scholar 

  • Nagao R, Kagatani K, Ueno Y, Shen J-R, Akimoto S (2019a) Ultrafast excitation energy dynamics in a diatom photosystem I-antenna complex: a femtosecond fluorescence upconversion study. J Phys Chem B 123:2673–2678

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Ueno Y, Shen J-R, Akimoto S (2019b) Low-energy chlorophylls in fucoxanthin chlorophyll a/c-binding protein conduct excitation energy transfer to photosystem I in diatoms. J Phys Chem B 123:66–70

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Yokono M, Ueno Y, Shen J-R, Akimoto S (2019c) pH-sensing machinery of excitation energy transfer in diatom PSI-FCPI complexes. J Phys Chem Lett 10:3531–3535

    Article  CAS  PubMed  Google Scholar 

  • Nagao R, Kato K, Ifuku K, Suzuki T, Kumazawa M, Uchiyama I, Kashino Y, Dohmae N, Akimoto S, Shen J-R, Miyazaki N, Akita F (2020a) Structural basis for assembly and function of a diatom photosystem I-light-harvesting supercomplex. Nat Commun 11:2481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagao R, Ueno Y, Akimoto S, Shen J-R (2020b) 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, 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 

  • 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 

  • Nikolova D, Weber D, Scholz M, Bald T, Scharsack JP, Hippler M (2017) Temperature-induced remodeling of the photosynthetic machinery tunes photosynthesis in the thermophilic alga Cyanidioschyzon merolae. Plant Physiol 174:35–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pi X, Tian L, Dai H-E, Qin X, Cheng L, Kuang T, Sui S-F, Shen J-R (2018) Unique organization of photosystem I-light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc Natl Acad Sci U S A 115:4423–4428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polívka T, Sundström V (2004) Ultrafast dynamics of carotenoid excited states−From solution to natural and artificial systems. Chem Rev 104:2021–2072

    Article  PubMed  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 

  • Tan S, Wolfe GR, Cunningham FX Jr, Gantt E (1995) Decrease of polypeptides in the PS I antenna complex with increasing growth irradiance in t the red alga Porphyridium cruentum. Photosynth Res 45:1–10

    Article  CAS  PubMed  Google Scholar 

  • Thangaraj B, Jolley CC, Sarrou I, Bultema JB, Greyslak J, Whitelegge JP, Lin S, Kouřil R, Subramanyam R, Boekema EJ, Fromme P (2011) Efficient light harvesting in a dark, hot, acidic environment: the structure and function of PSI-LHCI from Galdieria sulphuraria. Biophys J 100:135–143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian L, Liu Z, Wang F, Shen L, Chen J, Chang L, Zhao S, Han G, Wang W, Kuang T, Qin X, Shen J-R (2017) Isolation and characterization of PSI-LHCI super-complex and their sub-complexes from a red alga Cyanidioschyzon merolae. Photosynth Res 133:201–214

    Article  CAS  PubMed  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 

  • Wientjes E, van Stokkum IHM, van Amerongen H, Croce R (2011) The role of the individual Lhcas in photosystem I excitation energy trapping. Biophys J 101:745–754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolfe GR, Cunningham FX Jr, Grabowski B, Gantt E (1994) Isolation and characterization of Photosystems I and II from the red alga Porphyridium cruentum. Biochim Biophys Acta, Bioenerg 1188:357–366

    Article  Google Scholar 

  • Xu C, Pi X, Huang Y, Han G, Chen X, Qin X, Huang G, Zhao S, Yang Y, Kuang T, Wang W, Sui S-F, Shen J-R (2020) Structural basis for energy transfer in a huge diatom PSI-FCPI supercomplex. Nat Commun 11:5081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon HS, Zuccarello GC, Bhattacharya D (2010) Evolutionary history and taxonomy of red algae. In: Seckbach J, Chapman DJ (eds) Red algae in the genomic age. Springer, Dordrecht, pp 25–42

    Chapter  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 for her assistance in this study. This work was supported by JSPS KAKENHI grant Nos. JP21K19085 (R.N.), JP20H02914 (K.K.), and JP17H06434 and JP22H04916 (J.-R.S.).

Funding

This study was supported by Japan Society for the Promotion of Science (Grant Nos. JP21K19085, JP20H02914, JP17H06434, JP22H04916).

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Author notes

  1. Ryo Nagao

    Present address: Faculty of Agriculture, Shizuoka University, Shizuoka-shi, Shizuoka, 422-8529, Japan

  2. Yoshifumi Ueno

    Present address: Institute of Arts and Science, Tokyo University of Science, Shinjyuku-ku, Tokyo, 162-8601, Japan

Authors and Affiliations

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

    Ryo Nagao & Jian-Ren Shen

  2. Graduate School of Science, Kobe University, Kobe-shi, Hyogo, 657-8501, Japan

    Yoshifumi Ueno, Miyu Furutani & Seiji Akimoto

  3. Structural Biology Division, Japan Synchrotron Radiation Research Institute (JASRI), Sayo-Gun, Hyogo, 679-5198, Japan

    Koji Kato

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  1. Ryo Nagao
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Contributions

R.N. conceived the project; R.N. purified the three types of preparations and analyzed their biochemical characterization; R.N. measured absorption and fluorescence spectra; Y.U. measured time-resolved fluorescence; M.F. and S.A. analyzed time-resolved fluorescence data; R.N., K.K., J.-R.S., and S.A. provided experimental and funding resources; and R.N. and S.A. wrote the manuscript, and all of the authors joined the discussion of the results.

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Correspondence to Ryo Nagao or Seiji Akimoto.

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Nagao, R., Ueno, Y., Furutani, M. et al. Biochemical and spectroscopic characterization of PSI-LHCI from the red alga Cyanidium caldarium. Photosynth Res 156, 315–323 (2023). https://doi.org/10.1007/s11120-023-00999-y

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