Abstract
CO2 concentration and temperature for growth of photosynthetic organisms are two important factors to ensure better photosynthetic performance. In this study, we investigated the effects of CO2 concentration and temperature on the photosynthetic performance in a marine centric diatom Chaetoceros gracilis. Cells were grown under four different conditions, namely, at 25 °C with air bubbling, at 25 °C with a supplementation of 3% CO2, at 30 °C with air bubbling, and at 30 °C with the CO2 supplementation. It was found that the growth rate of cells at 30 °C with the CO2 supplementation is faster than those at other three conditions. The pigment compositions of cells grown under the different conditions are altered, and fluorescence spectra measured at 77 K also showed different peak positions. A novel fucoxanthin chlorophyll a/c-binding protein complex is observed in the cells grown at 30 °C with the CO2 supplementation but not in the other three types of cells. Since oxygen-evolving activities of the four types of cells are almost unchanged, it is suggested that the CO2 supplementation and growth temperature are involved in the regulation of photosynthetic light-harvesting apparatus in C. gracilis at different degrees. Based on these observations, we discuss the favorable growth conditions for C. gracilis.
Similar content being viewed by others
Abbreviations
- Chl:
-
Chlorophyll
- FCP:
-
Fucoxanthin chlorophyll a/c-binding protein
- Mes:
-
2-(N-Morpholino)ethanesulfonic acid
- PS:
-
Photosystem
References
Akimoto S, Ueno Y, Yokono M, Shen J-R, Nagao R (2020) Adaptation of light-harvesting and energy-transfer processes of a diatom Chaetoceros gracilis to different light qualities. Photosynth Res. https://doi.org/10.1007/s11120-020-00713-2
Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180
Casazza AP, Szczepaniak M, Müller MG, Zucchelli G, Holzwarth AR (2010) Energy transfer processes in the isolated core antenna complexes CP43 and CP47 of photosystem II. Biochim Biophys Acta 1797:1606–1616
Croce R, Zucchelli G, Garlaschi FM, Jennings RC (1998) A thermal broadening study of the antenna chlorophylls in PSI-200, LHCI, and PSI core. Biochemistry 37:17355–17360
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240
Gao K, Campbell DA (2014) Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review. Funct Plant Biol 41:449–459
Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131
Groot M-L, Peterman EJG, van Stokkum IHM, Dekker JP, van Grondelle R (1995) Triplet and fluorescing states of the CP47 antenna complex of photosystem II studied as a function of temperature. Biophys J 68:281–290
Ihalainen JA, van Stokkum IHM, Gibasiewicz K, Germano M, van Grondelle R, Dekker JP (2005) Kinetics of excitation trapping in intact Photosystem I of Chlamydomonas reinhardtii and Arabidopsis thaliana. Biochim Biophys Acta 1706:267–275
Ikeda Y, Komura M, Watanabe M, Minami C, Koike H, Itoh S, Kashino Y, Satoh K (2008) Photosystem I complexes associated with fucoxanthin-chlorophyll-binding proteins from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 1777:351–361
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
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanzen 167:191–194
Lavaud J, Lepetit B (2013) An explanation for the inter-species variability of the photoprotective non-photochemical chlorophyll fluorescence quenching in diatoms. Biochim Biophys Acta 1827:294–302
Matsuda Y, Hopkinson BM, Nakajima K, Dupont CL, Tsuji Y (2017) Mechanisms of carbon dioxide acquisition and CO2 sensing in marine diatoms: a gateway to carbon metabolism. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2016.0403
Mimuro M, Akimoto S, Tomo T, Yokono M, Miyashita H, Tsuchiya T (2007) Delayed fluorescence observed in the nanosecond time region at 77 K originates directly from the photosystem II reaction center. Biochim Biophys Acta 1767:327–334
Mimuro M, Yokono M, Akimoto S (2010) Variations in photosystem I properties in the primordial cyanobacterium Gloeobacter violaceus PCC 7421. Photochem Photobiol 86:62–69
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 1767:1353–1362
Nagao R, Kato K, Suzuki T, Ifuku K, Uchiyama I, Kashino Y, Dohmae N, Akimoto S, Shen J-R, Miyazaki N, Akita F (2019a) Structural basis for energy harvesting and dissipation in a diatom PSII-FCPII supercomplex. Nat Plants 5:890–901
Nagao R, Takahashi S, Suzuki T, Dohmae N, Nakazato K, Tomo T (2013a) Comparison of oligomeric states and polypeptide compositions of fucoxanthin chlorophyll a/c-binding protein complexes among various diatom species. Photosynth Res 117:281–288
Nagao R, Tomo T, Narikawa R, Enami I, Ikeuchi M (2013b) Light-independent biosynthesis and assembly of the photosystem II complex in the diatom Chaetoceros gracilis. FEBS Lett 587:1340–1345
Nagao R, Tomo T, Noguchi E, Nakajima S, Suzuki T, Okumura A, Kashino Y, Mimuro M, Ikeuchi M, Enami I (2010) Purification and characterization of a stable oxygen-evolving Photosystem II complex from a marine centric diatom, Chaetoceros gracilis. Biochim Biophys Acta 1797:160–166
Nagao R, Tomo T, Noguchi E, Suzuki T, Okumura A, Narikawa R, Enami I, Ikeuchi M (2012) Proteases are associated with a minor fucoxanthin chlorophyll a/c-binding protein from the diatom, Chaetoceros gracilis. Biochim Biophys Acta 1817:2110–2117
Nagao R, Ueno Y, Akita F, Suzuki T, Dohmae N, Akimoto S, Shen J-R (2019b) Biochemical characterization of photosystem I complexes having different subunit compositions of fucoxanthin chlorophyll a/c-binding proteins in the diatom Chaetoceros gracilis. Photosynth Res 140:141–149
Nagao R, Ueno Y, Yokono M, Shen J-R, Akimoto S (2018) Alterations of pigment composition and their interactions in response to different light conditions in the diatom Chaetoceros gracilis probed by time-resolved fluorescence spectroscopy. Biochim Biophys Acta 1859:524–530
Nagao R, Ueno Y, Yokono M, Shen JR, Akimoto S (2019c) Effects of excess light energy on excitation-energy dynamics in a pennate diatom Phaeodactylum tricornutum. Photosynth Res 141:355–365
Nagao R, Yokono M, Akimoto S, Tomo T (2013c) High excitation energy quenching in fucoxanthin chlorophyll a/c-binding protein complexes from the diatom Chaetoceros gracilis. J Phys Chem B 117:6888–6895
Nagao R, Yokono M, Tomo T, Akimoto S (2014) Control mechanism of excitation energy transfer in a complex consisting of photosystem II and fucoxanthin chlorophyll a/c-binding protein. J Phys Chem Lett 5:2983–2987
Nagao R, Yokono M, Ueno Y, Shen J-R, Akimoto S (2019d) 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
Pi X, Zhao S, Wang W, Liu D, Xu C, Han G, Kuang T, Sui S-F, Shen J-R (2019) The pigment-protein network of a diatom photosystem II-light-harvesting antenna supercomplex. Science 365: eaax4406
Shibata Y, Nishi S, Kawakami K, Shen J-R, Renger T (2013) Photosystem II does not possess a simple excitation energy funnel: Time-resolved fluorescence spectroscopy meets theory. J Am Chem Soc 135:6903–6914
Slavov C, Ballottari M, Morosinotto T, Bassi R, Holzwarth AR (2008) Trap-limited charge separation kinetics in higher plant photosystem I complexes. Biophys J 94:3601–3612
Taddei L, Chukhutsina VU, Lepetit B, Stella GR, Bassi R, van Amerongen H, Bouly J-P, Jaubert M, Finazzi G, Falciatore A (2018) Dynamic changes between two LHCX-related energy quenching sites control diatom photoacclimation. Plant Physiol 177:953–965
Ueno Y, Nagao R, Shen J-R, Akimoto S (2019) Spectral properties and excitation relaxation of novel fucoxanthin chlorophyll a/c-binding protein complexes. J Phys Chem Lett 10:5148–5152
Yokono M, Nagao R, Tomo T, Akimoto S (2015) Regulation of excitation energy transfer in diatom PSII dimer: How does it change the destination of excitation energy? Biochim Biophys Acta 1847:1274–1282
Yokono M, Tomo T, Nagao R, Ito H, Tanaka A, Akimoto S (2012) Alterations in photosynthetic pigments and amino acid composition of D1 protein change energy distribution in photosystem II. Biochim Biophys Acta 1817:754–759
Acknowledgements
This work was supported by the Grants-in-Aid for Scientific Research from Japan Society for the Promotion of Science JP17K07442 and JP19H04726 (to R. N.), JP16H06553 (to S. A.), and JP17H06433 (to J.-R. S.).
Author information
Authors and Affiliations
Corresponding authors
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
Nagao, R., Ueno, Y., Akimoto, S. et al. Effects of CO2 and temperature on photosynthetic performance in the diatom Chaetoceros gracilis. Photosynth Res 146, 189–195 (2020). https://doi.org/10.1007/s11120-020-00729-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-020-00729-8