Process intensification for the enhancement of growth and chlorophyll molecules of isolated Chlorella thermophila: A systematic experimental and optimization approach

References

• Hossain, N.; Zaini, J.; Mahlia, T. M. I. Experimental Investigation of Energy Properties for Stigonematales sp. Microalgae as Potential Biofuel Feedstock. Int. J. Sustain. Eng. 2019, 12, 123–130. DOI: 10.1080/19397038.2018.1521882.
   Web of Science ®Google Scholar
• Hossain, N.; Zaini, J.; Mahlia, T. M. I.; Azad, A. K. Elemental, Morphological and Thermal Analysis of Mixed Microalgae Species from Drain Water. Renew. Energy. 2019, 131, 617–624. DOI: 10.1016/j.renene.2018.07.082.
   Web of Science ®Google Scholar
• Kumar, R. A Review on the Modelling of Hydrothermal Liquefaction of Biomass and Waste Feedstocks. Energy Nexus 2022, 5, 100042. DOI: 10.1016/j.nexus.2022.100042.
   Google Scholar
• Clark, M. Handbook of Textile and Industrial Dyeing: Principles, Processes and Types of Dyes; Elsevier: Amsterdam, The Netherlands, 2011.
   Google Scholar
• Khanra, S.; Mondal, M.; Halder, G.; Tiwari, O. N.; Gayen, K.; Bhowmick, T. K. Downstream Processing of Microalgae for Pigments, Protein and Carbohydrate in Industrial Application: A Review. Food Bioprod. Process. 2018, 110, 60–84. DOI: 10.1016/j.fbp.2018.02.002.
   Web of Science ®Google Scholar
• Viera, I.; Pérez-Gálvez, A.; Roca, M. Green Natural Colorants. Molecules 2019, 24, 154. DOI: 10.3390/molecules24010154.
   PubMed Web of Science ®Google Scholar
• Kustov, A. V.; Belykh, D. V.; Smirnova, N. L.; Venediktov, E. A.; Kudayarova, T. V.; Kruchin, S. O.; Khudyaeva, I. S.; Berezin, D. B. Synthesis and Investigation of Water-Soluble Chlorophyll Pigments for Antimicrobial Photodynamic Therapy. Dyes Pigm. 2018, 149, 553–559. DOI: 10.1016/j.dyepig.2017.09.073.
   Web of Science ®Google Scholar
• Hosikian, A.; Lim, S.; Halim, R.; Danquah, M. K. Chlorophyll Extraction from Microalgae: A Review on the Process Engineering Aspects. Int. J. Chem. Eng. 2010, 2010, 1–11. DOI: 10.1155/2010/391632.
   Google Scholar
• Park, J.; Craggs, R.; Shilton, A. Wastewater Treatment High Rate Algal Ponds for Biofuel Production. Bioresour. Technol. 2011, 102, 35–42. DOI: 10.1016/j.biortech.2010.06.158.
   PubMed Web of Science ®Google Scholar
• Juneja, A.; Ceballos, R. M.; Murthy, G. S. Effects of Environmental Factors and Nutrient Availability on the Biochemical Composition of Algae for Biofuels Production: A Review. Energies 2013, 6, 4607–4638. DOI: 10.3390/en6094607.
   Web of Science ®Google Scholar
• Gonçalves, A. L.; Pires, J. C.; Simoes, M. The Effects of Light and Temperature on Microalgal Growth and Nutrient Removal: An Experimental and Mathematical Approach. RSC Adv. 2016, 6, 22896–22907. DOI: 10.1039/C5RA26117A.
   Web of Science ®Google Scholar
• Amini Khoeyi, Z.; Seyfabadi, J.; Ramezanpour, Z. Effect of Light Intensity and Photoperiod on Biomass and Fatty Acid Composition of the Microalgae, Chlorella vulgaris. Aquacult. Int. 2012, 20, 41–49. DOI: 10.1007/s10499-011-9440-1.
   Web of Science ®Google Scholar
• Ghosh, A.; Khanra, S.; Mondal, M.; Devi, T. I.; Halder, G.; Tiwari, O. N.; Bhowmick, T. K.; Gayen, K. Biochemical Characterization of Microalgae Collected from North East Region of India Advancing Towards the Algae‐Based Commercial Production. Asia-Pac. J. Chem. Eng. 2017, 12, 745–754. DOI: 10.1002/apj.2114.
   Web of Science ®Google Scholar
• Bohutskyi, P.; Kligerman, D. C.; Byers, N.; Nasr, L. K.; Cua, C.; Chow, S.; Su, C.; Tang, Y.; Betenbaugh, M. J.; Bouwer, E. J.; et al. Effects of Inoculum Size, Light Intensity, and Dose of Anaerobic Digestion Centrate on Growth and Productivity of Chlorella and Scenedesmus Microalgae and Their Poly-Culture in Primary and Secondary Wastewater. Algal. Res. 2016, 19, 278–290. DOI: 10.1016/j.algal.2016.09.010.
   Google Scholar
• Singh, R.; Upadhyay, A. K.; Chandra, P.; Singh, D. P. Sodium Chloride Incites Reactive Oxygen Species in Green Algae Chlorococcum humicola and Chlorella vulgaris: Implication on Lipid Synthesis, Mineral Nutrients and Antioxidant System. Bioresour. Technol. 2018, 270, 489–497. DOI: 10.1016/j.biortech.2018.09.065.
   PubMed Web of Science ®Google Scholar
• Asada, K. The Water-Water Cycle in Chloroplasts: Scavenging of Active Oxygens and Dissipation of Excess Photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 601–639. DOI: 10.1146/annurev.arplant.50.1.601.
   PubMed Web of Science ®Google Scholar
• Demidchik, V.; Straltsova, D.; Medvedev, S. S.; Pozhvanov, G. A.; Sokolik, A.; Yurin, V. Stress-Induced Electrolyte Leakage: The Role of K+-Permeable Channels and Involvement in Programmed Cell Death and Metabolic Adjustment. J. Exp. Bot. 2014, 65, 1259–1270. DOI: 10.1093/jxb/eru004.
   PubMed Web of Science ®Google Scholar
• Ji, X.; Cheng, J.; Gong, D.; Zhao, X.; Qi, Y.; Su, Y.; Ma, W. The Effect of NaCl Stress on Photosynthetic Efficiency and Lipid Production in Freshwater Microalga—Scenedesmus obliquus XJ002. Sci. Total Environ. 2018, 633, 593–599. DOI: 10.1016/j.scitotenv.2018.03.240.
   PubMed Web of Science ®Google Scholar
• Prakasham, R.; Rao, C. S.; Sarma, P. Green Gram Husk—An Inexpensive Substrate for Alkaline Protease Production by Bacillus sp. in Solid-State Fermentation. Bioresour. Technol. 2006, 97, 1449–1454. DOI: 10.1016/j.biortech.2005.07.015.
   PubMed Web of Science ®Google Scholar
• Prakasham, R. S.; Rao, C. S.; Rao, R. S.; Lakshmi, G. S.; Sarma, P. N. L‐Asparaginase Production by Isolated Staphylococcus sp.–6A: Design of Experiment considering Interaction Effect for Process Parameter Optimization. J. Appl. Microbiol. 2007, 102, 1382–1391. DOI: 10.1111/j.1365-2672.2006.03173.x.
   PubMed Web of Science ®Google Scholar
• Himabindu, M.; Ravichandra, P.; Vishalakshi, K.; Jetty, A. Optimization of Critical Medium Components for the Maximal Production of Gentamicin by Micromonospora echinospora ATCC 15838 Using Response Surface Methodology. Appl. Biochem. Biotechnol. 2006, 134, 143–154. DOI: 10.1385/ABAB:134:2:143.
   PubMed Web of Science ®Google Scholar
• Houng, J.-Y.; Liao, J.-H.; Wu, J.-Y.; Shen, S.-C.; Hsu, H.-F. Enhancement of Asymmetric Bioreduction of Ethyl 4-Chloro Acetoacetate by the Design of Composition of Culture Medium and Reaction Conditions. Process. Biochem. 2007, 42, 1–7. DOI: 10.1016/j.procbio.2006.03.035.
   Web of Science ®Google Scholar
• Baishan, F.; Hongwen, C.; Xiaolan, X.; Ning, W.; Zongding, H. Using Genetic Algorithms Coupling Neural Networks in a Study of Xylitol Production: Medium Optimisation. Process. Biochem. 2003, 38, 979–985.
   Web of Science ®Google Scholar
• Rao, R.; Prakasham, R. S.; Prasad, K.; Rajesham, S.; Sarma, P. N.; Rao, L. Xylitol Production by Candida sp.: Parameter Optimization Using Taguchi Approach. Process. Biochem. 2004, 39, 951–956. DOI: 10.1016/S0032-9592(03)00207-3.
   Web of Science ®Google Scholar
• Arulsudar, N.; Subramanian, N.; Murthy, R. Comparison of Artificial Neural Network and Multiple Linear Regression in the Optimization of Formulation Parameters of Leuprolide Acetate Loaded Liposomes. J. Pharm. Pharm. Sci. 2005, 8, 243–258.
   PubMed Web of Science ®Google Scholar
• Žužek, M.; Friedrich, J.; Cestnik, B.; Karalič, A.; Cimerman, A. Optimization of Fermentation Medium by a Modified Method of Genetic Algorithms. Biotechnol. Tech. 1996, 10, 991–996. DOI: 10.1007/BF00180409.
   Google Scholar
• Rao, C. S.; Sathish, T.; Mahalaxmi, M.; Laxmi, G. S.; Rao, R. S.; Prakasham, R. S. Modelling and Optimization of Fermentation Factors for Enhancement of Alkaline Protease Production by Isolated Bacillus circulans Using Feed‐Forward Neural Network and Genetic Algorithm. J. Appl. Microbiol. 2008, 104, 889–898. DOI: 10.1111/j.1365-2672.2007.03605.x.
   PubMed Web of Science ®Google Scholar
• Kumar, V.; Muthuraj, M.; Palabhanvi, B.; Ghoshal, A. K.; Das, D. High Cell Density Lipid Rich Cultivation of a Novel Microalgal Isolate Chlorella Sorokiniana FC6 IITG in a Single-Stage Fed-Batch Mode under Mixotrophic Condition. Bioresour. Technol. 2014, 170, 115–124. DOI: 10.1016/j.biortech.2014.07.066.
   PubMed Web of Science ®Google Scholar
• Berman-Frank, I.; Lundgren, P.; Chen, Y. B.; Küpper, H.; Kolber, Z.; Bergman, B.; Falkowski, P. Segregation of Nitrogen Fixation and Oxygenic Photosynthesis in the Marine Cyanobacterium trichodesmium. Science 2001, 294, 1534–1537. DOI: 10.1126/science.1064082.
   PubMed Web of Science ®Google Scholar
• Carvalho, A. P.; Meireles, L. A.; Malcata, F. X. Microalgal Reactors: A Review of Enclosed System Designs and Performances. Biotechnol. Prog. 2006, 22, 1490–1506. DOI: 10.1002/bp060065r.
   PubMed Web of Science ®Google Scholar
• Garzón-Castro, C. L.; Cortés-Romero, J. A.; Arcos-Legarda, J.; Tello, E. Optimal Decision Curve of Light Intensity to Maximize the Biomass Concentration in a Batch Culture. Biochem. Eng. J. 2017, 123, 57–65. DOI: 10.1016/j.bej.2017.04.001.
   Web of Science ®Google Scholar
• Ghosh, A.; Sarkar, S.; Gayen, K.; Bhowmick, T. K. Effects of Carbon, Nitrogen, and Phosphorus Supplements on Growth and Biochemical Composition of Podohedriella sp. (MCC44) Isolated from Northeast India. Environ. Prog. Sustain. Energy 2020, 39, e13378.
   Web of Science ®Google Scholar
• Sarkar, S.; Manna, M. S.; Bhowmick, T. K.; Gayen, K. Priority-Based Multiple Products from Microalgae: Review on Techniques and Strategies. Crit. Rev. Biotechnol. 2020, 40, 590–607. DOI: 10.1080/07388551.2020.1753649.
   PubMed Web of Science ®Google Scholar
• Mondal, M.; Ghosh, A.; Tiwari, O. N.; Gayen, K.; Das, P.; Mandal, M. K.; Halder, G. Influence of Carbon Sources and Light Intensity on Biomass and Lipid Production of Chlorella Sorokiniana BTA 9031 Isolated from Coalfield Under Various Nutritional Modes. Energy Convers. Manag. 2017, 145, 247–254. DOI: 10.1016/j.enconman.2017.05.001.
   Web of Science ®Google Scholar
• Lichtenthaler, H. K. Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods Enzymol. 1987, 148, 350–382.
   Web of Science ®Google Scholar
• Pancha, I.; Chokshi, K.; Maurya, R.; Trivedi, K.; Patidar, S. K.; Ghosh, A.; Mishra, S. Salinity Induced Oxidative Stress Enhanced Biofuel Production Potential of Microalgae Scenedesmus sp. CCNM 1077. Bioresour. Technol. 2015, 189, 341–348. DOI: 10.1016/j.biortech.2015.04.017.
   PubMed Web of Science ®Google Scholar
• Coleman, M. C.; Buck, K. K.; Block, D. E. An Integrated Approach to Optimization of Escherichia coli Fermentations Using Historical Data. Biotechnol. Bioeng. 2003, 84, 274–285. DOI: 10.1002/bit.10719.
   PubMed Web of Science ®Google Scholar
• Roy, S.; Banerjee, R.; Bose, P. K. Performance and Exhaust Emissions Prediction of a CRDI Assisted Single Cylinder Diesel Engine Coupled with EGR Using Artificial Neural Network. Appl. Energy 2014, 119, 330–340. DOI: 10.1016/j.apenergy.2014.01.044.
   Web of Science ®Google Scholar
• Sarkar, S.; Mankad, J.; Padhihar, N.; Manna, M. S.; Bhowmick, T. K.; Gayen, K. Enhancement of Growth and Biomolecules (Carbohydrates, Proteins, and Chlorophylls) of Isolated Chlorella thermophila Using Optimization Tools. Prep. Biochem. Biotechnol. 2022, 1–17. DOI: 10.1080/10826068.2022.2033995.
   PubMed Web of Science ®Google Scholar
• White, D. A.; Pagarette, A.; Rooks, P.; Ali, S. T. The Effect of Sodium Bicarbonate Supplementation on Growth and Biochemical Composition of Marine Microalgae Cultures. J. Appl. Phycol. 2013, 25, 153–165. DOI: 10.1007/s10811-012-9849-6.
   Web of Science ®Google Scholar
• Taguchi, G. Introduction to Quality Engineering: Designing Quality into Products and Processes; The Organization: Tokyo, Japan, 1986.
   Google Scholar
• Difusa, A.; Talukdar, J.; Kalita, M. C.; Mohanty, K.; Goud, V. V. Effect of Light Intensity and pH Condition on the Growth, Biomass and Lipid Content of Microalgae Scenedesmus Species. Biofuels 2015, 6, 37–44. DOI: 10.1080/17597269.2015.1045274.
   Web of Science ®Google Scholar
• Xu, Y.; Ibrahim, I. M.; Harvey, P. J. The Influence of Photoperiod and Light Intensity on the Growth and Photosynthesis of Dunaliella salina (Chlorophyta) CCAP 19/30. Plant Physiol. Biochem. 2016, 106, 305–315. DOI: 10.1016/j.plaphy.2016.05.021.
   PubMed Web of Science ®Google Scholar
• Mulders, K. J. M.; Lamers, P. P.; Martens, D. E.; Wijffels, R. H. Phototrophic Pigment Production with Microalgae: Biological Constraints and Opportunities. J. Phycol. 2014, 50, 229–242. DOI: 10.1111/jpy.12173.
   PubMed Web of Science ®Google Scholar
• Eze, V. C.; Velasquez-Orta, S. B.; Hernández-García, A.; Monje-Ramírez, I.; Orta-Ledesma, M. T. Kinetic Modelling of Microalgae Cultivation for Wastewater Treatment and Carbon Dioxide Sequestration. Algal Res. 2018, 32, 131–141. DOI: 10.1016/j.algal.2018.03.015.
   Google Scholar
• Münkel, R.; Schmid-Staiger, U.; Werner, A.; Hirth, T. Optimization of Outdoor Cultivation in Flat Panel Airlift Reactors for Lipid Production by Chlorella vulgaris. Biotechnol. Bioeng. 2013, 110, 2882–2893. DOI: 10.1002/bit.24948.
   PubMed Web of Science ®Google Scholar
• Singh, S.; Singh, P. Effect of Temperature and Light on the Growth of Algae Species: A Review. Renew. Sustain. Energy Rev. 2015, 50, 431–444. DOI: 10.1016/j.rser.2015.05.024.
   Web of Science ®Google Scholar
• Gupta, B.; Huang, B. Mechanism of Salinity Tolerance in Plants: Physiological, Biochemical, and Molecular Characterization. Int. J. Genomics. 2014, 2014, 701596. DOI: 10.1155/2014/701596.
   PubMed Web of Science ®Google Scholar
• Periasamy, R.; Palvannan, T. Optimization of Laccase Production by Pleurotus ostreatus IMI 395545 Using the Taguchi DOE Methodology. J. Basic Microbiol. 2010, 50, 548–556. DOI: 10.1002/jobm.201000095.
   PubMed Web of Science ®Google Scholar
• Shahbazian, A.; Navarchian, A. H.; Pourmehr, M. Application of Taguchi Method to Investigate the Effects of Process Factors on the Performance of Batch Emulsion Polymerization of Vinyl Chloride. J. Appl. Polym. Sci. 2009, 113, 2739–2746. DOI: 10.1002/app.30194.
   Web of Science ®Google Scholar
• Molloy, C.; Syrett, P. Interrelationships between Uptake of Urea and Uptake of Ammonium by Microalgae. J. Exp. Mar. Biol. Ecol. 1988, 118, 85–95. DOI: 10.1016/0022-0981(88)90232-8.
   Web of Science ®Google Scholar
• Solomon, C. M.; Glibert, P. M. Urease Activity in Five Phytoplankton Species. Aquat. Microb. Ecol. 2008, 52, 149–157. DOI: 10.3354/ame01213.
   Web of Science ®Google Scholar
• Yu, B. S.; Sung, Y. J.; Hong, M. E.; Sim, S. J. Improvement of Photoautotrophic Algal Biomass Production after Interrupted CO2 Supply by Urea and KH2PO4 Injection. Energies 2021, 14, 778. DOI: 10.3390/en14030778.
   Web of Science ®Google Scholar
• Flynn, K. J.; Butler, I. Nitrogen Sources for the Growth of Marine Microalgae: Role of Dissolved Free Amino Acids. Mar. Ecol. Prog. Ser. 1986, 34, 281–304. DOI: 10.3354/meps034281.
   Web of Science ®Google Scholar
• Berman-Frank, I.; Lundgren, P.; Falkowski, P. Nitrogen Fixation and Photosynthetic Oxygen Evolution in Cyanobacteria. Res. Microbiol. 2003, 154, 157–164. DOI: 10.1016/S0923-2508(03)00029-9.
   PubMed Web of Science ®Google Scholar
• Chiranjeevi, P.; Mohan, S. V. Critical Parametric Influence on Microalgae Cultivation towards Maximizing Biomass Growth with Simultaneous Lipid Productivity. Renew. Energy 2016, 98, 64–71. DOI: 10.1016/j.renene.2016.03.063.
   Web of Science ®Google Scholar
• Markou, G.; Depraetere, O.; Muylaert, K. Effect of Ammonia on the Photosynthetic Activity of Arthrospira and Chlorella: A Study on Chlorophyll Fluorescence and Electron Transport. Algal Res. 2016, 16, 449–457. DOI: 10.1016/j.algal.2016.03.039.
   Google Scholar
• Muthuraj, M.; Kumar, V.; Palabhanvi, B.; Das, D. Evaluation of Indigenous Microalgal Isolate Chlorella sp. FC2 IITG as a Cell Factory for Biodiesel Production and Scale up in Outdoor Conditions. J. Ind. Microbiol. Biotechnol. 2014, 41, 499–511. DOI: 10.1007/s10295-013-1397-9.
   PubMed Web of Science ®Google Scholar
• Morales-Sánchez, D.; Tinoco-Valencia, R.; Kyndt, J.; Martinez, A. Heterotrophic Growth of Neochloris Oleoabundans Using Glucose as a Carbon Source. Biotechnol. Biofuels. 2013, 6, 100–113. DOI: 10.1186/1754-6834-6-100.
   PubMed Web of Science ®Google Scholar
• Radkova, M.; Stoyneva-Gärtner, M.; Dincheva, I.; Stoykova, P.; Uzunov, B.; Dimitrova, P.; Borisova, C.; Gärtner, G. Chlorella vulgaris H1993 and Desmodesmus communis H522 for Low-Cost Production of High-Value Microalgal Products. Biotechnol. Biotechnol. Equip. 2019, 33, 243–249. DOI: 10.1080/13102818.2018.1562381.
   Web of Science ®Google Scholar