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Outdoor photoacclimation of two Chlorella strains characterized by normal and reduced light-harvesting antennas: photosynthetic activity and chlorophyll-protein organization

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Abstract

Photoacclimation of two Chlorella cultures – strain g-120 characterised by a reduced size of light-harvesting antenna complex (LHC) and strain R-117 with full antenna size was studied during 5-day outdoor trials. The aim was to correlate the functional and structural changes in the photosynthetic apparatus to culture growth, photochemical activity and thylakoid composition of chlorophyll (Chl)-protein complexes and corresponding polypeptides. Chlorella g-120 was characterized by a low Chl/biomass ratio (< 0.5% of dry weight), about four times lower compared to Chlorella R-117. The important observation was that the high molecular mass Chl-binding protein supercomplexes, i.e. Photosystem II (PSII) and Photosystem I (PSI) cores associated with LHCs were physically missing or negligible in Chlorella g-120. However, there were no visible changes in Chl-protein composition in the g-120 strain during its acclimation to phototrophic conditions. Measurement of the effective absorption cross-section of PSII centres confirmed a markedly reduced functional antenna size in Chlorella g-120 as compared to R-117 which coincided with the absence of the PSII-LHC supercomplexes. We demonstrated that Chlorella g-120 represents a typical reduced antenna-size strain due to its Chl-protein composition. As compared to the full-antenna Chlorella R-117 strain, the outdoor cultures of Chlorella g-120 showed significantly lower oxygen production and electron transport rate measured in-situ. On the contrary, Chlorella g-120 revealed increased futile energy dissipation via non-photochemical quenching and higher respiration compared to Chlorella R-117. Consequently, the potential use of microalgae strains with reduced LHCII for outdoor mass cultivation may not be as straightforward as anticipated from laboratory experiments.

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References

  • Babaei A, Ranglová K, Malapascua JR, Torzillo G, Shayegan J, Silva Benavides AM, Masojídek J (2020) Photobiochemical changes in Chlorella g120 culture during trophic conversion (metabolic pathway shift) from heterotrophic to phototrophic growth regime. J Appl Phycol 32:2807–2818

    Article  CAS  Google Scholar 

  • Ballottari M, Girardon J, Dall'Osto L, Bassi R (2012) Evolution and functional properties of Photosystem II light harvesting complexes in eukaryotes. Biochim Biophys Acta 1817:143–157

    Article  CAS  PubMed  Google Scholar 

  • Benemann J (1989) The future of microalgal biotechnology. In: Cresswell R, Rees T, Shah N (eds) Algal and Cyanobacteria Biotechnology. Longman Scientific, New York, pp 317–337

    Google Scholar 

  • Boekema EJ, van Roon H, van Breemen JFL, Dekker JP (1999) Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur J Biochem 266:444–452

    Article  CAS  PubMed  Google Scholar 

  • Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R (2011a) Analysis of LHcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol 9:e1000577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonente G, Formighieri C, Mantelli M, Catalanotti C, Giuliano G, Morosinotto T, Bassi R (2011b) Mutagenesis and phenotypic selection as a strategy toward domestication of Chlamydomonas reinhardtii strains for improved performance in photobioreactors. Photosynth Res 108:107–120

    Article  CAS  PubMed  Google Scholar 

  • Cazzaniga S, Dall’Osto L, Szaub J, Scibilia L, Ballottari M, Purton S, Bassi R (2014) Domestication of the green alga Chlorella sorokiniana: reduction of antenna size improves light-use efficiency in a photobioreactor. Biotechnol Biofuels 7:157–170

    Article  PubMed  PubMed Central  Google Scholar 

  • Cazzaniga S, Kim M, Bellamoli F, Jeong J, Lee S, Perozeni F, Pompa A, Jin E-S Ballottari M (2020) Photosystem II antenna complexes CP26 and CP29 are essential for nonphotochemical quenching in Chlamydomonas reinhardtii. Plant Cell Environ 43:496–509

    Article  CAS  PubMed  Google Scholar 

  • Chow Y, Thung L (2015) Quantifying the competitive advantage of light green algal cells in batch culture. J Appl Phycol 27:1805–1812

    Article  CAS  Google Scholar 

  • Dall’Osto L, Cazzaniga S, Guardini Z, Barera S, Benedetti M, Mannino G, Maffei ME, Bassi R (2019) Combined resistance to oxidative stress and reduced antenna size enhance light-to-biomass conversion efficiency in Chlorella vulgaris cultures. Biotechnol Biofuels 12:221

    Article  PubMed  PubMed Central  Google Scholar 

  • De Mooij T, Janssen M, Cerezo-Chinarro O, Mussgnug JH (2015) Antenna size reduction as a strategy to increase biomass productivity: a great potential not yet realized. J Appl Phycol 27:1063–1077

    Article  Google Scholar 

  • De Mooij T, Schediwy K, Wijffels RH, Janssen M (2016) Modeling the competition between antenna size mutant and wild type microalgae in outdoor mass culture. Aust J Biotechnol 240:1–13

    Article  Google Scholar 

  • Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta Bioenerg 1847:468–485

    Article  CAS  Google Scholar 

  • Doucha J, Lívanský K (1995) Novel outdoor thin-layer high-density microalgal culture system: productivity and operation parameters. Algol Stud 76:129–147

    Google Scholar 

  • Drop B, Webber-Birungi M, Yadav Sathish KN, 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

    Article  CAS  PubMed  Google Scholar 

  • Elrad D (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Formighieri C, Franck F, Bassi R (2012) Regulation of the pigment optical density of an algal cell: filling the gap between photosynthetic productivity in the laboratory and in mass culture. J Biotechnol 162:115–123

    Article  CAS  PubMed  Google Scholar 

  • Gordon JM, Polle JEW (2007) Ultrahigh bioproductivity from algae. Appl Microbiol Biotechnol 76:969–975

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Ruban A (2005) Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56:365–373

    Article  CAS  PubMed  Google Scholar 

  • Huesemann MH, Hausmann TS, Bartha R, Aksoy M, Weissman JC, Benemann J (2009) Biomass productivities in wild type and pigment mutant of Cyclotella sp. (Diatom). Appl Biochem Biotechnol 157:507–526

    Article  CAS  PubMed  Google Scholar 

  • Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NP (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98:565–574

    Article  CAS  PubMed  Google Scholar 

  • Jerez CG, Malapascua JR, Sergejevova M, Masojidek J, Figueroa FL (2016) Chlorella fusca (Chlorophyta) grown in thin-layer cascades: Estimation of biomass productivity by in-vivo chlorophyll a fluorescence monitoring. Algal Res 17:21–30

    Article  Google Scholar 

  • Kirst H, Garcia-Cerdan JG, Zurbriggen A, Ruehle T, Melis A (2012) Truncated photosystem chlorophyll antenna size in the green microalga Chlamydomonas reinhardtii upon deletion of the TLA3-CpSRP43 gene. Plant Physiol 160:2251–2260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klughammer C, Schreiber U (2008) Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the saturation pulse method. PAM Appl Notes 1:27–35

    Google Scholar 

  • Kolber ZS, Prasil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367:88–106

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Knoppová J, Krynická V, Nixon P, Tichý M (2010) Role of FtsH2 in the repair of the Photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster. Biochim Biophys Acta 1797:566–575

    Article  CAS  PubMed  Google Scholar 

  • Komenda J, Krynická V, Zachar T (2019) Isolation of thylakoid membranes from the cyanobacterium Synechocystis sp. PCC 6803 and analysis of their photosynthetic pigment-protein complexes by clear native-PAGE. Bio-Protocol 9:e3126

    Article  PubMed  PubMed Central  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kromkamp JC, Forster RM (2003) The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–111

    Article  Google Scholar 

  • Kwon J-H, Bernát G, Wagner H, Rögner M, Rexroth S (2013) Reduced light-harvesting antenna: consequences on cyanobacterial metabolism and photosynthetic productivity. Algal Res 2:188–195

    Article  Google Scholar 

  • Malapascua JRF, Jerez CG, Sergejevová M, Figueroa FL, Masojídek J (2014) Photosynthesis monitoring to optimize the growth of microalgal mass cultures: application of chlorophyll fluorescence techniques. Aquat Biol 22:124–140

    Article  Google Scholar 

  • Malapascua JR, Ranglová K, Masojídek J (2019) Photosynthesis and growth kinetics of Chlorella vulgaris R-117 cultured in an internally LED-illuminated photobioreactor. Photosynthetica 57:103–112

    Article  CAS  Google Scholar 

  • Masojídek J, Kopecký J, Giannelli L, Torzillo G (2011a) Productivity correlated to photobiochemical performance of Chlorella mass cultures grown outdoors in thin-layer cascades. J Ind Microbiol Biotechnol 38:307–317

    Article  PubMed  Google Scholar 

  • Masojídek J, Vonshak A, Torzillo G (2011b) Chlorophyll fluorescence applications in microalgal mass cultures. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Developments in Applied Phycology, vol 4. Springer, Dordrecht, pp 277–292

  • Masojídek J, Sergejevová M, Malapascua JR, Kopecký J (2015) Thin-layer systems for mass cultivation of microalgae: flat panels and sloping cascades. In: Bajpai R, Prokop A, Zappi M (eds) Algal Biorefinery, vol 2. Springer, Cham, pp 237–262

    Chapter  Google Scholar 

  • Masojídek J, Ranglová K, Rearte TA, Celis Plá PSM, Torzillo G, Benavides AMS, Neori A, Gómez C, Álvarez-Gómez F, Lukeš M, Caporgno MP, Abdala R, Miazek K, Massocato TF, da Silva JC, Atzmüller R, Al Mahrouqui H, Estrella FS, Figueroa FL (2021) Changes in photosynthesis, growth and biomass composition in outdoor Chlorella g-120 culture during the metabolic shift from heterotrophic to phototrophic cultivation regime. Algal Res 56:102303

  • Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177:272–280

    Article  CAS  Google Scholar 

  • Melis A, Neidhardt J, Benemann JR (1998) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibits higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10:515–525

    Article  Google Scholar 

  • Mitra M, Kirst H, Dewez D, Melis A (2012) Modulation of the light-harvesting chlorophyll antenna size in Chlamydomonas reinhardtii by TLA1 gene over-expression and RNA interference. Philos Trans R Soc B 367:3430–3443

    Article  CAS  Google Scholar 

  • Mussgnug JH, Wobbe L, Elles I, Claus C, Hamilton M, Fink A, Kahmann U, Kapazoglou A, Mullineaux CW, Hippler M, Nickelsen J, Nixon PJ, Kruse O (2005) NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell 17:3409–3421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mussgnug JH, Thomas-Hall S, Rupprecht J, Foo A, Klassen V, McDowall A, Schenk PM, Kruse O, Hankamer B (2007) Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 5:802–814

    Article  CAS  PubMed  Google Scholar 

  • Nakajima Y, Ueda R (1997) Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments. J Appl Phycol 9:503–510

    CAS  Google Scholar 

  • Nakajima Y, Ueda R (1999) Improvement of microalgal photosynthetic productivity by reducing the content of light harvesting pigment. J Appl Phycol 11:195–201

    Article  Google Scholar 

  • Nakajima Y, Ueda R (2000) The effect of reducing light-harvesting pigment on marine microalgal productivity. J Appl Phycol 12:285–290

    Article  CAS  Google Scholar 

  • Ort DR, Zhu X, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85

    Article  CAS  PubMed  Google Scholar 

  • Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521

    Article  CAS  PubMed  Google Scholar 

  • Perin G, Bellan A, Segalla A, Meneghesso A, Alboresi A, Morosinotto T (2015) Generation of random mutants to improve light-use efficiency of Nannochloropsis gaditana cultures for biofuel production. Biotechnol Biofuels 8:161

    Article  PubMed  PubMed Central  Google Scholar 

  • Perrine Z, Negi S, Sayre RT (2012) Optimization of photosynthetic light energy utilization by microalgae. Algal Res 1:134–142

    Article  Google Scholar 

  • Polle JEW, Benemann JR, Tanaka A, Melis A (2000) Photosynthetic apparatus organization and function in the wild type and a chlorophyll b-less mutant of Chlamydomonas reinhardtii. Dependence on carbon source. Planta 211:335–344

    Article  CAS  PubMed  Google Scholar 

  • Polle J, Kanakagiri S, Jin E, Masuda T, Melis A (2002) Truncated chlorophyll antenna size of the photosystems—a practical method to improve microalgal productivity and hydrogen production in mass culture. Int J Hydrog Energy 27:1257–1264

    Article  CAS  Google Scholar 

  • Polle JEW, Kanakagiri SD, Melis A (2003) tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 217:49–59

    Article  CAS  PubMed  Google Scholar 

  • Ranglová K, Lakatos GE, Câmara Manoel JA, Grivalský T, Masojídek J (2019) Rapid screening test to estimate temperature optima for microalgae growth using photosynthesis activity measurements. Folia Microbiol 64:615–625

    Article  Google Scholar 

  • Rearte TA, Celis-Plá P, Neori A, Masojídek J, Torzillo G, Gómez C, Silva Benavides AM, Álvarez-Gómez F, Abdala Diaz R, Ranglova K, Caporgno M, Favero Massocato T, Caemo da Silva J, Al Mahrouqui H, Atzmüller R, Figueroa F (2021) Photosynthetic performance of Chlorella vulgaris R117 mass culture is moderated by diurnal oxygen gradients in an outdoor thin layer cascade. Algal Res 54:102176

  • Richmond A (2013) Biological principles of mass cultivation of photoautotrophic microalgae. In: Richmond A, Hu Q (eds) Handbook of Microalgal Culture: Applied Phycology and Biotechnology. Wiley-Blackwell, Chichester, pp 171–204

    Chapter  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CD (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181

    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 

  • Schramm A, Jakob T, Wilhelm C (2016) The impact of the optical properties and respiration of algal cells with truncated antennae on biomass production under simulated outdoor conditions. Curr Biotech 5:142–153

    Article  CAS  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U, Endo T, Mi H, Asada K (1995) Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant Cell Physiol 36:873–882

    Article  CAS  Google Scholar 

  • Sergejevová M, Malapascua JR, Kopecký J, Masojídek J (2015) Photobioreactors with internal illumination. In: Bajpai R, Prokop A, Zappi M (eds) Algal Biorefinery, vol 2. Springer, Cham, pp 237–262

    Google Scholar 

  • Shen L, Huang L, Chang S, Wang W, Wang J, Kuang T, Han G, Shen J-R, Zhang X (2019) Structure of a C2S2M2N2-type PSII–LHCII supercomplex from the green alga Chlamydomonas reinhardtii. PNAS 116:21246–21255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shin W-S, Lee B, Jeong B-R, Chang JK, Kwon J-H (2016) Truncated light-harvesting chlorophyll antenna size in Chlorella vulgaris improves biomass productivity. J Appl Phycol 28:3193–3202

    Article  CAS  Google Scholar 

  • Touloupakis E, Faraloni C, Silva Benavides AM, Masojidek J, Torzillo G (2021) Sustained photobiological hydrogen production by Chlorella vulgaris without nutrient starvation. Int J Hydrog Energy 46:3684–3694

    Article  CAS  Google Scholar 

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  PubMed  Google Scholar 

  • Vecchi V, Barera S, Bassi R, Dall’Osto L (2020) Potential and challenges of improving photosynthesis in algae. Plants 9:1–25

    Article  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolutions. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Whitmarsh JH, Eckert J, Schoneich C, Renger G (1993) Functional size of photosystem II determined by radiation inactivation. Photosynth Res 38:363–368

    Article  CAS  PubMed  Google Scholar 

  • Wobbe L, Blifernez O, Schwarz C, Mussgnug JH, Nickelsen J, Kruse O (2009) Cysteine modification of a specific repressor protein controls the translational status of nucleus-encoded LHCII mRNAs in Chlamydomonas. Proc Natl Acad Sci U S A 106:13290–13295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaťková I, Sergejevová M, Urban J, Vachta R, Štys D, Masojídek J (2011) Carotenoid-enriched microalgal biomass as feed supplement for freshwater ornamentals: albinic form of Wels catfish (Silurus glanis). Aquac Nutr 17:278–286

    Article  Google Scholar 

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Acknowledgements

The authors thank Ms Soňa Pekařová, Ms Nastasia Kastiukovich and Mr Thomas Loussier for technical assistance and Dr Radek Kaňa for discussion.

Funding

This research was funded by the Technology Agency of the Czech Republic, programme National Centres of Competence (grant TN010000048/03) and in part by the EU H2020 programme, project SABANA (grant no.727874).

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Authors and Affiliations

  1. Centre ALGATECH, Institute of Microbiology, CZ-37981, Třeboň, Czech Republic

    Jiří Masojídek, Karolína Ranglová, Martina Bečková, Jana Knoppová, Filip Charvát & Josef Komenda

  2. Faculty of Science, University of South Bohemia, CZ-37005, České Budějovice, Czech Republic

    Jiří Masojídek, Filip Charvát & Josef Komenda

  3. CIMAR – Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, San Pedro, Costa Rica

    Giuseppe Torzillo

  4. CNR - Institute of Bioeconomy, Sesto Fiorentino, Firenze, Italy

    Giuseppe Torzillo

  5. Escuela de Biologia, CIMAR – Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, San Pedro, Costa Rica

    Ana Margarita Silva Benavides

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  1. Jiří Masojídek
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  2. Karolína Ranglová
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  6. Ana Margarita Silva Benavides
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  8. Josef Komenda
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Contributions

Conceptualization, JM, KR, GT, JoK; methodology, JM, KR, JoK, JaK, GT, AMSB; investigation, KR, JM, GT, MB, AMSB, JaK, FC; data curation, KR, AMSB, JM, FC, MB, JaK; writing & original draft preparation, JM, KR; review and editing, KR, GT, JoK; visualization, KR, JM, JoK, JaK, FC; supervision, JM, JoK, GT; funding acquisition, JM, GT, JoK. All authors have read and agreed to the published version of the manuscript.

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Masojídek, J., Ranglová, K., Bečková, M. et al. Outdoor photoacclimation of two Chlorella strains characterized by normal and reduced light-harvesting antennas: photosynthetic activity and chlorophyll-protein organization. J Appl Phycol 34, 2339–2353 (2022). https://doi.org/10.1007/s10811-022-02803-1

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