Abstract
Light-harvesting complex II (LHCII) absorbs light energy and transfers it primarily to photosystem II in green algae and land plants. Although the trimeric structure of LHCII is conserved between the two lineages, its subunit composition and function are believed to differ significantly. In this study, we purified four LHCII trimers from the green alga Chlamydomonas reinhardtii and analyzed their biochemical properties. We used several preparation methods to obtain four distinct fractions (fractions 1–4), each of which contained an LHCII trimer with different contents of Type I, III, and IV proteins. The pigment compositions of the LHCIIs in the four fractions were similar. The absorption and fluorescence spectra were also similar, although the peak positions differed slightly. These results indicate that this green alga contains four types of LHCII trimer with different biochemical and spectroscopic features. Based on these findings, we discuss the function and structural organization of green algal LHCII antennae.
Similar content being viewed by others
Abbreviations
- CBB:
-
Coomassie brilliant blue
- Chl:
-
Chlorophyll
- CV:
-
Column volume
- α-DDM:
-
Dodecyl-α-D-maltoside
- β-DDM:
-
Dodecyl-β-D-maltoside
- LHCII:
-
Light-harvesting complex II
- MES:
-
2-(N-morpholino) ethanesulfonic acid
- PSII:
-
Photosystem II
- PSI:
-
Photosystem I
- SDG:
-
Sucrose density gradient
- SDS-PAGE:
-
Sodium dodecyl sulfate–polyacrylamide gel electrophoresis
- UPLC:
-
Ultra-performance liquid chromatography
References
Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: differential analysis of the Lhcb1-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43:9467–9476
Drop B, Webber-Birungi M, Yadav SKN, Filipowicz-Szymanska A, Fusetti F, Boekema EJ, Croce R (2014) Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii. Biochim Biophys Acta 1837:63–72
Elrad D, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816
Ferrante P, Ballottari M, Bonente G, Giuliano G, Bassi R (2012) LHCBM1 and LHCBM2/7 polypeptides, components of major LHCII complex, have distinct functional roles in photosynthetic antenna system of Chlamydomonas reinhardtii. J Biol Chem 287:16276–16288
García-Cerdán JG, Kovács L, Tõth T et al (2011) The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants. Plant J 65:368–381
Gorman DS, Levine RP (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 54:1665–1669
Grewe S, Ballottari M, Alcocer M et al (2014) Light-harvesting complex protein LHCBM9 is critical for photosystem II activity and hydrogen production in Chlamydomonas reinhardtii. Plant Cell 26:1598–1611
Gulis G, Narasimhulu KV, Redding KE (2008) Purification of His(6)-tagged photosystem I from Chlamydomonas reinhardtii. Photosynth Res 96:51–60
Ikeuchi M, Inoue Y (1988) A new 4.8-kDa polypeptide intrinsic to the PS II reaction center, as revealed by modified SDS-PAGE with improved resolution of low-molecular-weight proteins. Plant Cell Physiol 29:1233–1239
Jackowski G, Kacprzak K, Jansson S (2001) Identification of Lhcb1/Lhcb2/Lhcb3 heterotrimers of the main light-harvesting chlorophyll a/bprotein complex II of Photosystem II (LHCII). Biochim Biophys Acta 1504:340–345
Janik E, Bednarska J, Sowinski K, Luchowski R, Zubik M, Grudzinski W, Gruszecki WI (2017) Light-induced formation of dimeric LHCII. Photosynth Res 132:265–276
Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lamb JJ, Røkke G, Hohmann-Marriott MF (2018) Chlorophyll fluorescence emission spectroscopy of oxygenic organisms at 77 K. Photosynthetica 56:105–124
Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428:287–292
Minagawa J, Takahashi Y (2004) Structure, function and assembly of Photosystem II and its light-harvesting proteins. Photosynth Res 82:241–263
Natali A, Croce R (2015) Characterization of the major light-harvesting complexes (LHCBM) of the green alga Chlamydomonas reinhardtii. PLoS ONE 10:1–18
Nguyen AV, Thomas-Hall SR, Malnoë A et al (2008) Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot Cell 7:1965–1979
Standfuss J, Van Scheltinga ACT, Lamborghini M, Kühlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J 24:919–928
Su X, Ma J, Wei X, Cao P, Zhu D, Chang W, Liu Z, Zhang X, Mei L (2017) Structure and assembly mechanism of plant C2S2M2-type PSII-LHCII supercomplex. Science 357:815–820
Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:477–482
Takahashi H, Okamuro A, Minagawa J, Takahashi Y (2014) Biochemical characterization of photosystem I-associated light-harvesting complexes I and II isolated from state 2 cells of Chlamydomonas reinhardtii. Plant Cell Physiol 55:1437–1449
Tokutsu R, Minagawa J (2013) Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 110:10016–10021
Tokutsu R, Kato N, Bui KH, Ishikawa T, Minagawa J (2012) Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem 287:31574–31581
Wei X, Su X, Cao P, Liu X, Chang W, Li M, Zhang X, Liu Z (2016) Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution. Nature 534:69–74
Wittig I, Braun HP, Schägger H (2006) Blue native PAGE. Nat Protoc 1:418–428
Acknowledgements
We thank Ms. Rie Uno (Osaka City University), Mr. Daisuke Namba (Osaka City University), and Ms. Chiyo Noda (National Institute for Basic Biology) for their assistance with purification and analysis. We are also grateful to Prof. Nobuo Kamiya (Osaka City University) and Associate Prof. Ikuko Miyahara (Osaka City University) for providing laboratory access. This work was funded by the Joint Usage/Research Program of the Artificial Photosynthesis, Osaka City University. K.K. and J.M. are grateful for the continued support of JST CREST, Japan (Grant No. JPMJCR13M4).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kawakami, K., Tokutsu, R., Kim, E. et al. Four distinct trimeric forms of light-harvesting complex II isolated from the green alga Chlamydomonas reinhardtii. Photosynth Res 142, 195–201 (2019). https://doi.org/10.1007/s11120-019-00669-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-019-00669-y