Use of an immobilised thermostable α-CA (SspCA) for enhancing the metabolic efficiency of the freshwater green microalga Chlorella sorokiniana

References

• Miner GL, Bauerle WL, Baldocchi DD. Estimating the sensitivity of stomatal conductance to photosynthesis: a review. Plant Cell Environ 2017;40:1214–38.
   PubMed Web of Science ®Google Scholar
• Niyogi KK. Editorial overview: physiology and metabolism: light responses from photoreceptors to photosynthesis and photoprotection. Curr Opin Plant Biol 2017;37:iv–vi.
   PubMed Web of Science ®Google Scholar
• Kumpers BM, Burgess SJ, Reyna-Llorens I, et al. Shared characteristics underpinning C4 leaf maturation derived from analysis of multiple C3 and C4 species of Flaveria. J Exp Bot 2017;68:177–89.
   PubMed Web of Science ®Google Scholar
• Reeves G, Grange-Guermente MJ, Hibberd JM. Regulatory gateways for cell-specific gene expression in C4 leaves with Kranz anatomy. J Exp Bot 2017;68:107–16.
   PubMed Web of Science ®Google Scholar
• Tcherkez G, Gauthier P, Buckley TN, et al. Leaf day respiration: low CO2 flux but high significance for metabolism and carbon balance. New Phytol 2017;216:986–1001.
   PubMed Web of Science ®Google Scholar
• Galmes J, Andralojc PJ, Kapralov MV, et al. Environmentally driven evolution of Rubisco and improved photosynthesis and growth within the C3 genus Limonium (Plumbaginaceae). New Phytol 2014;203:989–99.
   PubMed Web of Science ®Google Scholar
• Sage TL, Busch FA, Johnson DC, et al. Initial events during the evolution of C4 photosynthesis in C3 species of Flaveria. Plant Physiol 2013;163:1266–76.
   PubMed Web of Science ®Google Scholar
• Niklaus M, Kelly S. The molecular evolution of C4 photosynthesis: opportunities for understanding and improving the world’s most productive plants. J Exp Bot 2019;70:795–804.
   PubMed Web of Science ®Google Scholar
• Yamori W, Hikosaka K, Way DA. Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosyn Res 2014;119:101–17.
   PubMed Web of Science ®Google Scholar
• Ślesak I, Ślesak H, Kruk J. RubisCO early oxygenase activity: a kinetic and evolutionary perspective. Bioessays 2017;39:1700071.
   Web of Science ®Google Scholar
• Allakhverdiev SI, Kreslavski VD, Klimov VV, et al. Heat stress: an overview of molecular responses in photosynthesis. Photosyn Res 2008;98:541–50.
   PubMed Web of Science ®Google Scholar
• Giordano M, Beardall J, Raven JA. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 2005;56:99–131.
   PubMed Web of Science ®Google Scholar
• Kaplan A, Reinhold L. CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 1999;50:539–70.
   PubMed Web of Science ®Google Scholar
• Moroney JV, Jungnick N, Dimario RJ, Longstreth DJ. Photorespiration and carbon concentrating mechanisms: two adaptations to high O2, low CO2 conditions. Photosyn Res 2013;117:121–31.
   PubMed Web of Science ®Google Scholar
• Raven JA, Beardall J, Sanchez-Baracaldo P. The possible evolution and future of CO2-concentrating mechanisms. J Exp Bot 2017;68:3701–16.
   PubMed Web of Science ®Google Scholar
• Atkinson N, Feike D, Mackinder LC, et al. Introducing an algal carbon-concentrating mechanism into higher plants: location and incorporation of key components. Plant Biotechnol J 2016;14:1302–15.
   PubMed Web of Science ®Google Scholar
• Mackinder L. The Chlamydomonas CO2-concentrating mechanism and its potential for engineering photosynthesis in plants. New Phytol 2018;217:54–61.
   PubMed Web of Science ®Google Scholar
• Wang Y, Duanmu D, Spalding MH. Carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii: inorganic carbon transport and CO2 recapture. Photosyn Res 2011;109:115–22.
   PubMed Web of Science ®Google Scholar
• Alterio V, Langella E, Viparelli F, et al. Structural and inhibition insights into carbonic anhydrase CDCA1 from the marine diatom Thalassiosira weissflogii. Biochimie 2012;94:1232–41.
   PubMed Web of Science ®Google Scholar
• De Simone G, Supuran CT. (In)organic anions as carbonic anhydrase inhibitors. J Inorg Biochem 2012;111:117–29.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases as drug targets-an overview. Curr Top Med Chem 2007;7:825–33.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases-an overview. Curr Pharm Des 2008;14:603–14.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Scozzafava A. Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem 2007;15:4336–50.
   PubMed Web of Science ®Google Scholar
• Kinney JN, Axen SD, Kerfeld CA. Comparative analysis of carboxysome shell proteins. Photosyn Res 2011;109:21–32.
   PubMed Web of Science ®Google Scholar
• Turmo A, Gonzalez-Esquer CR, Kerfeld CA. Carboxysomes: metabolic modules for CO2 fixation. FEMS Microbiol Lett 2017;364: 364–70.
   Web of Science ®Google Scholar
• Kimber MS. Carboxysomal carbonic anhydrases. Subcell Biochem 2014;75:89–103.
   PubMedGoogle Scholar
• Price GD, Pengelly JJ, Forster B, et al. The cyanobacterial CCM as a source of genes for improving photosynthetic CO2 fixation in crop species. J Exp Bot 2013;64:753–68.
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, De Simone G, et al. Cloning, expression and purification of the complete domain of the eta-carbonic anhydrase from Plasmodium falciparum. J Enzyme Inhib Med Chem 2016;31:54–9.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Cloning, expression, purification and sulfonamide inhibition profile of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum. Bioorg Med Chem Lett 2016;26:4184–90.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Anion inhibition profiles of the complete domain of the η-carbonic anhydrase from Plasmodium falciparum. Bioorg Med Chem 2016;24:4410–4.
   PubMed Web of Science ®Google Scholar
• Annunziato G, Angeli A, D'Alba F, et al. Discovery of new potential anti-infective compounds based on carbonic anhydrase inhibitors by rational target-focused repurposing approaches. ChemMedChem 2016;11:1904–14.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Anion inhibition profiles of α-, β- and γ-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem 2016;24:3413–7.
   PubMed Web of Science ®Google Scholar
• Abdel Gawad NM, Amin NH, Elsaadi MT, et al. Synthesis of 4-(thiazol-2-ylamino)-benzenesulfonamides with carbonic anhydrase I, II and IX inhibitory activity and cytotoxic effects against breast cancer cell lines. Bioorg Med Chem 2016;24:3043–51.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the carbonic anhydrases from two pathogens of the oral cavity: Streptococcus mutans and Porphyromonas gingivalis. Curr Top Med Chem 2016;16:2359–68.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Comparison of the sulfonamide inhibition profiles of the α-, β- and γ-carbonic anhydrases from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem Lett 2016;26:1941–6.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites 2017;7:56.
   PubMed Web of Science ®Google Scholar
• Jensen EL, Clement R, Kosta A, et al. A new widespread subclass of carbonic anhydrase in marine phytoplankton. Isme J 2019;13:2094–106.
   PubMed Web of Science ®Google Scholar
• Kikutani S, Nakajima K, Nagasato C, et al. Thylakoid luminal θ-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci USA 2016;113:9828–33.
   PubMed Web of Science ®Google Scholar
• De Simone G, Di Fiore A, Capasso C, Supuran CT. The zinc coordination pattern in the η-carbonic anhydrase from Plasmodium falciparum is different from all other carbonic anhydrase genetic families. Bioorg Med Chem Lett 2015;25:1385–9.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. The η-class carbonic anhydrases as drug targets for antimalarial agents. Expert Opin Ther Targets 2015;19:551–63.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Fisher GM, et al. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum-the η-carbonic anhydrases. Bioorg Med Chem Lett 2014;24:4389–96.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Tolvanen ME, Ortutay C, Parkkila S. Carbonic anhydrase related proteins: molecular biology and evolution. Subcell Biochem 2014;75:135–56.
   PubMedGoogle Scholar
• Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the selectivity and efficiency of the bacterial carbonic anhydrase inhibitors. Curr Med Chem 2015;22:2130–9.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma-carbonic anhydrases from Bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem 2015;30:325–32.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Sulfa and trimethoprim-like drugs - antimetabolites acting as carbonic anhydrase, dihydropteroate synthase and dihydrofolate reductase inhibitors. J Enzyme Inhib Med Chem 2014;29:379–87.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Anti-infective carbonic anhydrase inhibitors: a patent and literature review. Expert Opin Ther Patents 2013;23:693–704.
   PubMed Web of Science ®Google Scholar
• Prete SD, Angeli A, Ghobril C, et al. Anion inhibition profile of the beta-carbonic anhydrase from the opportunist pathogenic Fungus Malassezia restricta involved in dandruff and seborrheic dermatitis. Metabolites 2019;9: 147–57.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Ghobril C, et al. Cloning, purification, and characterization of a beta-carbonic anhydrase from Malassezia restricta, an opportunistic pathogen involved in dandruff and seborrheic dermatitis. Int J Mol Sci 2019;20: 2447–59.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Bua S, Del Prete S, et al. Natural polyphenols selectively inhibit β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa: activity and modeling studies. ChemMedChem 2018;13:816–23.
   PubMed Web of Science ®Google Scholar
• Nocentini A, Vullo D, Del Prete S, et al. Inhibition of the β-carbonic anhydrase from the dandruff-producing fungus Malassezia globosa with monothiocarbamates. J Enzyme Inhib Med Chem 2017;32:1064–70.
   PubMed Web of Science ®Google Scholar
• Entezari Heravi Y, Bua S, Nocentini A, et al. Inhibition of Malassezia globosa carbonic anhydrase with phenols. Bioorg Med Chem 2017;25:2577–82.
   PubMed Web of Science ®Google Scholar
• Minhas AK, Hodgson P, Barrow CJ, Adholeya A. A review on the assessment of stress conditions for simultaneous production of microalgal lipids and carotenoids. Front Microbiol 2016;7: 546–64.
   PubMed Web of Science ®Google Scholar
• Carfagna S, Landi V, Coraggio F, et al. Different characteristics of C-phycocyanin (C-PC) in two strains of the extremophilic Galdieria phlegrea. Algal Res 2018;31:406–12.
   Google Scholar
• Bottone C, Camerlingo R, Miceli R, et al. Antioxidant and anti-proliferative properties of extracts from heterotrophic cultures of Galdieria sulphuraria. Nat Prod Res 2018;15:1–5.
   Google Scholar
• Carfagna S, Salbitani G, Bottone C, Vona V. Galdieria sulphuraria as a possible source of food colorant. J Nutr Ecol Food Res 2016;3:78–81.
   Google Scholar
• Mus F, Toussaint JP, Cooksey KE, et al. Physiological and molecular analysis of carbon source supplementation and pH stress-induced lipid accumulation in the marine diatom Phaeodactylum tricornutum. Appl Microbiol Biotechnol 2013;97:3625–42.
   PubMed Web of Science ®Google Scholar
• YuvrajPadmanabhan P. Technical insight on the requirements for CO2-saturated growth of microalgae in photobioreactors. 3 Biotech 2017;7:119.
   PubMedGoogle Scholar
• Fuentes JL, Garbayo I, Cuaresma M, et al. Impact of microalgae-bacteria interactions on the production of algal biomass and associated compounds. Mar Drugs 2016;14: 100–16.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Perfetto R, Rossi M, et al. A one-step procedure for immobilising the thermostable carbonic anhydrase (SspCA) on the surface membrane of Escherichia coli. J Enzyme Inhib Med Chem 2017;32:1120–8.
   PubMed Web of Science ®Google Scholar
• Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248–54.
   PubMed Web of Science ®Google Scholar
• Capasso C, De Luca V, Carginale V, et al. Biochemical properties of a novel and highly thermostable bacterial α-carbonic anhydrase from Sulfurihydrogenibium yellowstonense YO3AOP1. J Enzyme Inhib Med Chem 2012;27:892–7.
   PubMed Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680–5.
   PubMed Web of Science ®Google Scholar
• De Luca V, Del Prete S, Supuran CT, Capasso C. Protonography, a new technique for the analysis of carbonic anhydrase activity. J Enzyme Inhib Med Chem 2015;30:277–82.
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Iandolo E, et al. Protonography, a powerful tool for analyzing the activity and the oligomeric state of the γ-carbonic anhydrase identified in the genome of Porphyromonas gingivalis. Bioorg Med Chem 2015;23:3747–50.
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, Supuran CT, Capasso C. Protonography, a technique applicable for the analysis of η-carbonic anhydrase activity . J Enzyme Inhib Med Chem 2015;30:920–4.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Caminiti-Segonds N, et al. Protonography and anion inhibition profile of the α-carbonic anhydrase (CruCA4) identified in the Mediterranean red coral Corallium rubrum. Bioorg Chem 2018;76:281–7.
   PubMed Web of Science ®Google Scholar
• Salbitani G, Wirtz M, Hell R, Carfagna S. Affinity purification of O-acetylserine(thiol)lyase from Chlorella sorokiniana by recombinant proteins from Arabidopsis thaliana. Metabolites 2014;4:629–39.
   PubMedGoogle Scholar
• Inskeep WP, Bloom PR. Extinction coefficients of chlorophyll a and B in n,n-dimethylformamide and 80% acetone. Plant Physiol 1985;77:483–5.
   PubMed Web of Science ®Google Scholar
• Wellburn AR. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 1994;144:307–13.
   Web of Science ®Google Scholar
• Cullen JJ, Davis RF. The blank can make a big difference in oceanographic measurements. Limnol Oceanogr Bull 2003;12:29–35.
   Google Scholar
• Maxwell K, Johnson GN. Chlorophyll fluorescence-a practical guide. J Exp Bot 2000;51:659–68.
   PubMed Web of Science ®Google Scholar
• Moroney JV, Ma Y, Frey WD, et al. The carbonic anhydrase isoforms of Chlamydomonas reinhardtii: intracellular location, expression, and physiological roles. Photosyn Res 2011;109:133–49.
   PubMed Web of Science ®Google Scholar
• DiMario RJ, Machingura MC, Waldrop GL, Moroney JV. The many types of carbonic anhydrases in photosynthetic organisms. Plant Sci 2018;268:11–7.
   PubMed Web of Science ®Google Scholar
• Samukawa M, Shen C, Hopkinson BM, Matsuda Y. Localization of putative carbonic anhydrases in the marine diatom, Thalassiosira pseudonana. Photosyn. Res 2014;121:235–49.
   PubMed Web of Science ®Google Scholar
• Satoh A, Iwasaki T, Odani S, Shiraiwa Y. Purification, characterization and cDNA cloning of soluble carbonic anhydrase from Chlorella sorokiniana grown under ordinary air. Planta 1998;206:657–65.
   PubMed Web of Science ®Google Scholar
• Srinivasan R, Mageswari A, Subramanian P, et al. Bicarbonate supplementation enhances growth and biochemical composition of Dunaliella salina V-101 by reducing oxidative stress induced during macronutrient deficit conditions. Sci Rep 2018;8:6972.
   PubMed Web of Science ®Google Scholar
• Salbitani G, Barone CMA, Carfagna S. Effect of bicarbonate on growth of the oleaginous microalga Botryococcus braunii. Int J Plant Biol 2019;10: 35–7.
   Google Scholar
• Li J, Li C, Lan CQ, Liao D. Effects of sodium bicarbonate on cell growth, lipid accumulation, and morphology of Chlorella vulgaris. Microb Cell Fact 2018;17:111
   PubMed Web of Science ®Google Scholar
• Lohman EJ, Gardner RD, Pedersen T, et al. Optimized inorganic carbon regime for enhanced growth and lipid accumulation in Chlorella vulgaris. Biotechnol Biofuels 2015;8:82
   PubMed Web of Science ®Google Scholar
• Chiong MC, Meng CC, Cheng TC, et al. Liquid biofuels production and emissions performance in gas turbines: a review. Energy Conversion Manage 2018;173:640–58.
   Web of Science ®Google Scholar