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CO2 Supply Modulates Lipid Remodelling, Photosynthetic And bioRxiv preprint doi: https://doi.org/10.1101/2021.02.18.431842; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 1 CO2 supply modulates lipid remodelling, photosynthetic 2 and respiratory activities in Chlorella species 3 Michela Cecchin1, Matteo Paloschi1, Giovanni Busnardo1, Stefano Cazzaniga1, Stephan 4 Cuine2, Yonghua Li-Beisson2, Lutz Wobbe3 and Matteo Ballottari1* 5 6 1Dipartimento di Biotecnologie, Università di Verona, Strada Le Grazie 15, 37134 Verona, 7 Italy. 8 2Aix-Marseille Univ., CEA, CNRS, Institute of Biosciences and Biotechnologies of Aix- 9 Marseille, UMR7265, CEA Cadarache, Saint-Paul-lez Durance F-13108, France. 10 3Bielefeld University, Center for Biotechnology (CeBiTec), Faculty of Biology, 11 Universitätsstrasse 27, 33615, Bielefeld, Germany. 12 13 *Address for correspondence: [email protected] 14 15 Short title: Effects of different CO2 availability in Chlorella 16 17 One sentence summary: High/low CO2 availability induces cell responses as lipids 18 remodelling, adaptations of the photosynthetic apparatus and modulation of mitochondrial 19 respiration not conserved among green algae 20 21 Author contributions 22 M.B. conceived the work and designed the experimental plan. M.B., L.W. and Y.LB. 23 supervised experiments. M.C., M.P., G.B. and S.CA. performed experiments. Y.LB. and 24 S.CU. performed lipid analysis. L.W. provided assistance in the analysis of NAB1 in 25 Chlorella species. M. B. wrote the manuscript with the contribution of M.C., S.CA., L.W. and 26 Y.LB.. All the authors discussed the results, contributed to data interpretation, and 27 commented on the manuscript. 28 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.18.431842; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 29 ABSTRACT 30 Microalgae represent potential solutions to reduce the atmospheric CO2 level through 31 photosynthesis. To boost CO2 fixation by microalgae it is essential to understand physiologic 32 and metabolic responses at the base of CO2 assimilation and carbon flow. In this work two 33 Trebouxiophyceae species, Chlorella sorokiniana and Chlorella vulgaris, were investigated 34 for their metabolic responses to high and low CO2 (air level) availability. High CO2 35 availability resulted in an increase in biomass accumulation in both species but with a 36 different chloroplast and mitochondrial responses. In C. sorokiniana we observed increased 37 polar lipids and protein amount and a balanced NADPH redox state and a similar total 38 respiration in the two conditions analysed. In contrast, in C. vulgaris high CO2 level caused an 39 increase in TAG accumulation and a higher NADPH consumption suggesting a CO2 40 dependent increase of reducing power consumption in the chloroplast, which in turn 41 influences the redox state of the mitochondria by lowering total dark respiration. Several 42 rearrangements of the photosynthetic machinery were observed in both species, which differ 43 from those described for the model organism Chlamydomonas reinhardtii. In the case of C. 44 reinhardtii, adaptation of the photosynthetic apparatus to different CO2 availability relies on 45 the translational repressor NAB1. NAB1 homologous protein could be identified only in C. 46 vulgaris but lacked the regulation mechanisms previously described in C. reinhardtii. These 47 findings highlight that the acclimation strategies to cope with a fluctuating inorganic carbon 48 supply are diverse among green microalgae and point to new biotechnological strategies to 49 boost CO2 fixation. 50 51 INTRODUCTION 52 Microalgae emit half of the oxygen available in the atmosphere and contribute to half of the 53 total organic carbon produced worldwide (Li-Beisson et al., 2019; Salomé and Merchant, 54 2019). Thanks to the photosynthetic process algae convert light energy into chemical energy 55 to fix CO2 in organic compounds. Carbon dioxide is one of the main greenhouse gasses 56 responsible for global warming. CO2 level at the Earth’s surface atmosphere is constantly 57 increasing reaching 407.4 ± 0.1 ppm for 2018, an increase of 2.4 ± 0.1 ppm from 2017 58 (Dlugokencky, 2019). There is an urgent need for an efficient way to reduce the global carbon 59 footprint, which is fundamental to reduce the effects of human activity in the worldwide 60 poise. 61 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.18.431842; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 62 Microalgae are emerging as a possible solution due to their ability to grow at high levels of 63 CO2 and to produce biomass that can be exploited for several applications: as food or feed 64 supplement, biofuels or to produce high value products. Moreover, these photosynthetic 65 organisms do not require arable land, have a fast growth rate and waste products as well as 66 wastewater-derived effluent can be used as fertilizers for their cultivation (Lum et al., 2013). 67 68 Light is harvested in the microalgal chloroplast by pigment binding protein complexes called 69 Photosystem I (PSI) and II (PSII). These complexes are composed of a core complex, where 70 photochemical reactions occur, and an external antenna system which increases light 71 harvesting efficiency and where several photoprotective reactions occur (Gao et al., 2018; Pan 72 et al., 2019). In oxygenic photosynthetic organisms, as eukaryotic microalgae, PSI and PSII 73 work in series to strip electrons from water and transfer them to NADP+ producing NADPH. 74 During this linear electron transport protons are pumped from stroma to the lumen generating 75 an electrochemical gradient used by ATPase to synthetize ATP. ATP and NADPH are then 76 used by the Calvin Benson cycle to fix CO2 into sugars. In parallel, another electron transport 77 chain takes place in mitochondria, consuming oxygen and NADH and releasing NAD+ and 78 ATP. A constant balance between chloroplast and mitochondrial activity is fundamental for 79 cell survival and for adaptation to fluctuating environmental conditions. 80 81 It is important to point out that CO2 diffusion in the water environments, where microalgae 82 live, is strongly reduced compared to CO2 diffusion in air. CO2-limitation is known to reduce 83 the consumption of ATP and NADPH by the Calvin Benson cycle leading to an over-reduced 84 photosynthetic electron transport chain, which could potentially lead to oxidative stress 85 (Wang et al., 2015). For this reason several microalgae species evolved an efficient system to 86 enrich the CO2 level inside the cell, i.e. Carbon Concentrating Mechanism (CCM), a complex 87 mechanism by which inorganic carbon is actively transported close to the enzyme responsible 88 for its fixation, i.e. the RUBISCO enzyme (Wang et al., 2015). The CCM mechanism is 89 induced by low CO2 concentrations (air level or lower) (Wang et al., 2015). CO2 availability 90 plays thus a critical role in modulating photosynthetic efficiency and biomass accumulation in 91 microalgal cultures. For example, in the model green alga Chlamydomonas reinhardtii, CO2 92 has been reported to act as a molecular switch inducing a complex network of cell adaptation 93 mechanisms including a translational up-regulation in the formation of PSII antenna 94 complexes (Mussgnug et al., 2005; Wobbe et al., 2009; Berger et al., 2014; Berger et al., 95 2016; Blifernez-Klassen et al., 2021). In conditions of low CO2 availability, accumulation of 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.02.18.431842; this version posted February 19, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 96 the cytosolic RNA-binding protein NAB1 is triggered by the transcription factor LCRF (Low 97 Carbon dioxide Response Factor) (Blifernez-Klassen et al., 2021). NAB1 then represses the 98 translation of transcripts encoding light-harvesting antenna proteins (Mussgnug et al., 2005; 99 Berger et al., 2014). The translation repressor activity of NAB1 is controlled by two 100 independent mechanisms related to the methylation of Arg90 and Arg92 residues (Blifernez et 101 al., 2011) and to the redox state of Cys181 and Cys226 residues (Wobbe et al., 2009). NAB1 102 is highly active in the methylated state, while reduced Cys181 and reduced Cys226 are 103 required for NAB1 RNA-binding activity. Nitrosylation of Cys181 and Cys226 has also been 104 reported to inhibit the RNA binding activity of NAB1 (Berger et al., 2016). The truncation of 105 the PSII antenna reduces the excitation pressure on the photosynthetic apparatus as a response 106 to diminished CO2 availability (Berger et al., 2014). Accumulation of NAB1 and its post- 107 translational regulation have been demonstrated to be finely tuned as an acclimation 108 mechanism to different environmental conditions, including varying CO2 availability (Wobbe 109 et al., 2009; Berger et al., 2014; Berger et al., 2016). 110 111 Among microalgae species discovered, Trebouxiophyceae represent an evolutionary defined 112 class of green algae (Chlorophyta) comprising the green freshwater algae of the Chlorella 113 genus, one of the first microalgae to be cultured on a large scale due to their easy cultivation 114 and high resistance to stresses (Yang et al.
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