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Mixotrophic Cultivation of a Native Cyanobacterium, Pseudanabaena mucicola GO0704, to Produce Phycobiliprotein and Biodiesel

  • Kim, Shin Myung (Division of Environmental Science and Ecological Engineering, Korea University) ;
  • Bae, Eun Hee (Research Division of Microorganisms, National Institute of Biological Resources) ;
  • Kim, Jee Young (Division of Environmental Science and Ecological Engineering, Korea University) ;
  • Kang, Jae-Shin (Research Division of Microorganisms, National Institute of Biological Resources) ;
  • Choi, Yoon-E (Division of Environmental Science and Ecological Engineering, Korea University)
  • Received : 2022.07.05
  • Accepted : 2022.09.06
  • Published : 2022.10.28

Abstract

Global warming has accelerated in recent decades due to the continuous consumption of petroleum-based fuels. Cyanobacteria-derived biofuels are a promising carbon-neutral alternative to fossil fuels that may help achieve a cleaner environment. Here, we propose an effective strategy based on the large-scale cultivation of a newly isolated cyanobacterial strain to produce phycobiliprotein and biodiesel, thus demonstrating the potential commercial applicability of the isolated microalgal strain. A native cyanobacterium was isolated from Goryeong, Korea, and identified as Pseudanabaena mucicola GO0704 through 16s RNA analysis. The potential exploitation of P. mucicola GO0704 was explored by analyzing several parameters for mixotrophic culture, and optimal growth was achieved through the addition of sodium acetate (1 g/l) to the BG-11 medium. Next, the cultures were scaled up to a stirred-tank bioreactor in mixotrophic conditions to maximize the productivity of biomass and metabolites. The biomass, phycobiliprotein, and fatty acids concentrations in sodium acetate-treated cells were enhanced, and the highest biodiesel productivity (8.1 mg/l/d) was achieved at 96 h. Finally, the properties of the fuel derived from P. mucicola GO0704 were estimated with converted biodiesels according to the composition of fatty acids. Most of the characteristics of the final product, except for the cloud point, were compliant with international biodiesel standards [ASTM 6761 (US) and EN 14214 (Europe)].

Keywords

Acknowledgement

This work was supported by a grant from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR202112101).

References

  1. Quintana N, Van der Kooy F, Van de Rhee MD, Voshol GP, Verpoorte R. 2011. Renewable energy from Cyanobacteria: energy production optimization by metabolic pathway engineering. Appl. Microbiol. Biotechnol. 91: 471-490. https://doi.org/10.1007/s00253-011-3394-0
  2. Woodwell GM. 1989. The warming of the industrialized middle latitudes 1985-2050: Causes and consequences. Clim. Change 15: 31-50. https://doi.org/10.1007/BF00138844
  3. Malcolm JR, Liu C, Neilson RP, Hansen L, Hannah L. 2006. Global warming and extinctions of endemic species from biodiversity hotspots. Conserv. Biol. 20: 538-548. https://doi.org/10.1111/j.1523-1739.2006.00364.x
  4. Khasnis AA, Nettleman MD. 2005. Global warming and infectious disease. Arch. Med. Res. 36: 689-696. https://doi.org/10.1016/j.arcmed.2005.03.041
  5. Mata TM, Martins AA, Caetano NS. 2010. Microalgae for biodiesel production and other applications: A review. Renew. Sustain. Energy Rev. 14: 217-232. https://doi.org/10.1016/j.rser.2009.07.020
  6. Machado IM, Atsumi S. 2012. Cyanobacterial biofuel production. J. Biotechnol. 162: 50-56. https://doi.org/10.1016/j.jbiotec.2012.03.005
  7. Chisti Y. 2007. Biodiesel from microalgae. Biotechnol. Adv. 25: 294-306. https://doi.org/10.1016/j.biotechadv.2007.02.001
  8. Prasanna R, Renuka N, Nain L, Ramakrishnan B. 2021. Natural and constructed cyanobacteria-based consortia for enhancing crop growth and soil fertility, pp. 333-362. In Seneviratne G, Zavahir JS (eds.), Role of Microbial Communities for Sustainability, vol. 29. Springer, Singapore.
  9. Lau N-S, Matsui M, Abdullah AA-A. 2015. Cyanobacteria: photoautotrophic microbial factories for the sustainable synthesis of industrial products. Biomed Res. Int. 2015: 754934.
  10. Sivonen K. 1996. Cyanobacterial toxins and toxin production. Phycologia 35: 12-24. https://doi.org/10.2216/i0031-8884-35-6S-12.1
  11. Gantar M, Svircev Z. 2008. Microalgae and cyanobacteria: food for thought 1. J. Phycol. 44: 260-268. https://doi.org/10.1111/j.1529-8817.2008.00469.x
  12. Zeng Y, Tang J, Lian S, Tong D, Hu C. 2015. Study on the conversion of cyanobacteria of Taihu Lake water blooms to biofuels.Biomass Bioenergy 73: 95-101. https://doi.org/10.1016/j.biombioe.2014.12.007
  13. Jebali A, Acien F, Jimenez-Ruiz N, Gomez C, Fernandez-Sevilla J, Mhiri N, et al. 2019. Evaluation of native microalgae from Tunisia using the pulse-amplitude-modulation measurement of chlorophyll fluorescence and a performance study in semi-continuous mode for biofuel production. Biotechnol. Biofuels 12: 119. https://doi.org/10.1186/s13068-019-1461-4
  14. Abdelaziz AEM, Ghosh D, Hallenbeck PC. 2014. Characterization of growth and lipid production by Chlorella sp. PCH90, a microalga native to Quebec. Bioresour. Technol. 156: 20-28. https://doi.org/10.1016/j.biortech.2014.01.004
  15. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiol. 111: 1-61. https://doi.org/10.1099/00221287-111-1-1
  16. Ritchie RJ. 2006. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth. Res. 89: 27-41. https://doi.org/10.1007/s11120-006-9065-9
  17. Khatoon H, Kok Leong L, Abdu Rahman N, Mian S, Begum H, Banerjee S, et al. 2018. Effects of different light source and media on growth and production of phycobiliprotein from freshwater cyanobacteria. Bioresour. Technol. 249: 652-658. https://doi.org/10.1016/j.biortech.2017.10.052
  18. Cuellar-Bermudez SP, Magdalena JA, Muylaert K, Gonzalez-Fernandez C. 2019. High methane yields in anaerobic digestion of the cyanobacterium Pseudanabaena sp. Algal Res. 44: 101689. https://doi.org/10.1016/j.algal.2019.101689
  19. Marquez FJ, Sasaki K, Kakizono T, Nishio N, Nagai S. 1993. Growth characteristics of Spirulina platensis in mixotrophic and heterotrophic conditions. J. Ferment. Bioeng. 76: 408-410. https://doi.org/10.1016/0922-338X(93)90034-6
  20. D'Imporzano G, Silvia S, Davide V, Barbara S, Fabrizio A. 2017. Microalgae mixotrophic growth: opportunity for stream depuration and carbon recovery, pp. 141-177. In Tripathi B, Kumar D (eds.), Prospects and Challenges in Algal Biotechnology, Springer, Singapore.
  21. Chen T, Zheng W, Yang F, Bai Y, Wong Y-S. 2006. Mixotrophic culture of high selenium-enriched Spirulina platensis on acetate and the enhanced production of photosynthetic pigments. Enzyme Microb. Technol. 39: 103-107. https://doi.org/10.1016/j.enzmictec.2005.10.001
  22. Hassall K. 1958. Xylose as a specific inhibitor of photosynthesis. Nature 181: 1273-1274. https://doi.org/10.1038/1811273a0
  23. Cheng J, Fan W, Zheng L. 2021. Development of a mixotrophic cultivation strategy for simultaneous improvement of biomass and photosynthetic efficiency in freshwater microalga Scenedesmus obliquus by adding appropriate concentration of sodium acetate. Biochem. Eng. J. 176: 108177. https://doi.org/10.1016/j.bej.2021.108177
  24. Heinz S, Liauw P, Nickelsen J, Nowaczyk M. 2016. Analysis of photosystem II biogenesis in cyanobacteria. Biochim. Biophys. Acta Bioenerg. 1857: 274-287. https://doi.org/10.1016/j.bbabio.2015.11.007
  25. Kim DH, Kim JY, Oh J-J, Jeon MS, An HS, Jin CR, et al. 2021. A strategic approach to apply bacterial substances for increasing metabolite productions of Euglena gracilis in the bioreactor. Appl. Microbiol. Biotechnol. 105: 5395-5406. https://doi.org/10.1007/s00253-021-11412-w
  26. Lin Z, Raya A, Ju L-K. 2014. Microalga Ochromonas danica fermentation and lipid production from waste organics such as ketchup. Process Biochem. 49: 1383-1392. https://doi.org/10.1016/j.procbio.2014.05.015
  27. Patel BH. 2011. 11 - Natural dyes, pp. 395-424. In Clark M (ed.), Handbook of Textile and Industrial Dyeing, Woodhead Publishing Ltd., Cambridge, UK
  28. da Silva Ferreira V, Sant'Anna C. 2017. Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World J. Microbiol. Biotechnol. 33: 20. https://doi.org/10.1007/s11274-016-2181-6
  29. Caporgno MP, Haberkorn I, Bocker L, Mathys A. 2019. Cultivation of Chlorella protothecoides under different growth modes and its utilisation in oil/water emulsions. Bioresour. Technol. 288: 121476. https://doi.org/10.1016/j.biortech.2019.121476
  30. Liu X, Duan S, Li A, Xu N, Cai Z, Hu Z. 2009. Effects of organic carbon sources on growth, photosynthesis, and respiration of Phaeodactylum tricornutum. J. Appl. Phycol. 21: 239-246. https://doi.org/10.1007/s10811-008-9355-z
  31. Pagels F, Guedes AC, Amaro HM, Kijjoa A, Vasconcelos V. 2019. Phycobiliproteins from cyanobacteria: Chemistry and biotechnological applications. Biotechnol. Adv. 37: 422-443. https://doi.org/10.1016/j.biotechadv.2019.02.010
  32. Khoobkar Z, Delavari Amrei H. 2021. Effect of photo, hetero and mixotrophic conditions on the growth and composition of Anabaena variabilis: An energy nexus approach. Energy Nexus 2: 100010. https://doi.org/10.1016/j.nexus.2021.100010
  33. Parsaeimehr A, Ahmed II, Deumaga MLK, Hankoua B, Ozbay G. 2022. Enhancement in phycobiliprotein accumulation in Aphanothece sp. using different carbon sources and flashing frequency. Algal. Res. 66: 102805. https://doi.org/10.1016/j.algal.2022.102805
  34. Kaushal S, Singh Y, Khattar J, Singh D. 2017. Phycobiliprotein production by a novel cold desert cyanobacterium Nodularia sphaerocarpa PUPCCC 420.1. J. Appl. Phycol. 29: 1819-1827. https://doi.org/10.1007/s10811-017-1093-7
  35. Portillo FV-L, Sierra-Ibarra E, Vera-Estrella R, Revah S, Ramirez OT, Caspeta L, et al. 2022. Growth and phycocyanin production with Galdieria sulphuraria UTEX 2919 using xylose, glucose, and corn stover hydrolysates under heterotrophy and mixotrophy. Algal. Res. 65: 102752. https://doi.org/10.1016/j.algal.2022.102752
  36. Sloth JK, Wiebe MG, Eriksen NT. 2006. Accumulation of phycocyanin in heterotrophic and mixotrophic cultures of the acidophilic red alga Galdieria sulphuraria. Enzyme Microb. Technol. 38: 168-175. https://doi.org/10.1016/j.enzmictec.2005.05.010
  37. Abiusi F, Monino Fernandez P, Canziani S, Janssen M, Wijffels RH, Barbosa M. 2022. Mixotrophic cultivation of Galdieria sulphuraria for C-phycocyanin and protein production. Algal Res. 61: 102603. https://doi.org/10.1016/j.algal.2021.102603
  38. Rosa Cunha W, Godoy Cottas A, Azevedo Teixeira T, de Souza Ferreira J. 2020. Evaluation of phicocyanin produced by Anabaena variabilis using different organic carbon sources. J. Eng. Exact Sci. 6: 3.
  39. Jiang L, Wang Y, Yin Q, Liu G, Liu H, Huang Y, et al. 2017. Phycocyanin: a potential drug for cancer treatment. J. Cancer 8: 3416. https://doi.org/10.7150/jca.21058
  40. Huang A, Sun L, Wu S, Liu C, Zhao P, Xie X, et al. 2017. Utilization of glucose and acetate by Chlorella and the effect of multiple factors on cell composition. J. Appl. Phycol. 29: 23-33. https://doi.org/10.1007/s10811-016-0920-6
  41. Mondal M, Ghosh A, Sharma AS, Tiwari O, Gayen K, Mandal M, et al. 2016. Mixotrophic cultivation of Chlorella sp. BTA 9031 and Chlamydomonas sp. BTA 9032 isolated from coal field using various carbon sources for biodiesel production. Energy Convers. Manag. 124: 297-304. https://doi.org/10.1016/j.enconman.2016.07.033
  42. Griffiths MJ, Harrison ST. 2009. Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J. Appl. Phycol. 21: 493-507. https://doi.org/10.1007/s10811-008-9392-7
  43. Jung J-M, Kim JY, Jung S, Choi Y-E, Kwon EE. 2021. Quantitative study on lipid productivity of Euglena gracilis and its biodiesel production according to the cultivation conditions. J. Clean. Prod. 291: 125218. https://doi.org/10.1016/j.jclepro.2020.125218
  44. Lari Z, Abrishamchi P, Ahmadzadeh H, Soltani N. 2019. Differential carbon partitioning and fatty acid composition in mixotrophic and autotrophic cultures of a new marine isolate Tetraselmis sp. KY114885. J. Appl. Phycol. 31: 201-210. https://doi.org/10.1007/s10811-018-1549-4
  45. Baldisserotto C, Popovich C, Giovanardi M, Sabia A, Ferroni L, Constenla D, et al. 2016. Photosynthetic aspects and lipid profiles in the mixotrophic alga Neochloris oleoabundans as useful parameters for biodiesel production. Algal Res. 16: 255-265. https://doi.org/10.1016/j.algal.2016.03.022
  46. Liu L, Zhao Y, Jiang X, Wang X, Liang W. 2018. Lipid accumulation of Chlorella pyrenoidosa under mixotrophic cultivation using acetate and ammonium. Bioresour. Technol. 262: 342-346. https://doi.org/10.1016/j.biortech.2018.04.092
  47. Singhasuwan S, Choorit W, Sirisansaneeyakul S, Kokkaew N, Chisti Y. 2015. Carbon-to-nitrogen ratio affects the biomass composition and the fatty acid profile of heterotrophically grown Chlorella sp. TISTR 8990 for biodiesel production. J. Biotechnol. 216: 169-177. https://doi.org/10.1016/j.jbiotec.2015.10.003
  48. Lanjekar RD, Deshmukh D. 2016. A review of the effect of the composition of biodiesel on NOx emission, oxidative stability and cold flow properties. Renew. Sustain. Energy Rev. 54: 1401-1411. https://doi.org/10.1016/j.rser.2015.10.034
  49. Stansell GR, Gray VM, Sym SD. 2012. Microalgal fatty acid composition: implications for biodiesel quality. J. Appl. Phycol. 24: 791-801. https://doi.org/10.1007/s10811-011-9696-x
  50. Talebi AF, Tabatabaei M, Chisti Y. 2014. BiodieselAnalyzer: a user-friendly software for predicting the properties of prospective biodiesel. Biofuel Res. J. 1: 55-57.
  51. Hoekman SK, Broch A, Robbins C, Ceniceros E, Natarajan M. 2012. Review of biodiesel composition, properties, and specifications. Renew. Sustain. Energy Rev. 16: 143-169. https://doi.org/10.1016/j.rser.2011.07.143
  52. Knothe G. 2016. Chapter 2 - Biodiesel and Its Properties, pp. 15-42. In: McKeon TA, Hayes DG, Hildebrand DF, Weselake RJ (eds.), Industrial Oil Crops, AOCS Press.
  53. Shahabuddin M, Kalam MA, Masjuki HH, Bhuiya MMK, Mofijur M. 2012. An experimental investigation into biodiesel stability by means of oxidation and property determination. Energy 44: 616-622. https://doi.org/10.1016/j.energy.2012.05.032
  54. Saeedi Dehaghani AH, Rahimi R. 2019. An experimental study of diesel fuel cloud and pour point reduction using different additives. Petroleum 5: 413-416. https://doi.org/10.1016/j.petlm.2018.06.005
  55. Lee WS, Chua ASM, Yeoh HK, Ngoh GC. 2014. A review of the production and applications of waste-derived volatile fatty acids. Chem. Eng. J. 235: 83-99. https://doi.org/10.1016/j.cej.2013.09.002
  56. Li Y, He D, Niu D, Zhao Y. 2015. Acetic acid production from food wastes using yeast and acetic acid bacteria micro-aerobic fermentation. Bioprocess Biosyst. Eng. 38: 863-869. https://doi.org/10.1007/s00449-014-1329-8
  57. Sharma P, Gaur VK, Sirohi R, Varjani S, Kim SH, Wong JW. 2021. Sustainable processing of food waste for production of bio-based products for circular bioeconomy. Bioresour. Technol. 325: 124684. https://doi.org/10.1016/j.biortech.2021.124684
  58. Sharma YC, Singh B, Korstad J. 2011. A critical review on recent methods used for economically viable and eco-friendly development of microalgae as a potential feedstock for synthesis of biodiesel. Green Chem. 13: 2993-3006. https://doi.org/10.1039/c1gc15535k
  59. Yadav G, Sekar M, Kim S-H, Geo VE, Bhatia SK, Sabir JS, et al. 2021. Lipid content, biomass density, fatty acid as selection markers for evaluating the suitability of four fast growing cyanobacterial strains for biodiesel production. Bioresour. Technol. 325: 124654. https://doi.org/10.1016/j.biortech.2020.124654
  60. Anahas AMP, Muralitharan G. 2015. Isolation and screening of heterocystous cyanobacterial strains for biodiesel production by evaluating the fuel properties from fatty acid methyl ester (FAME) profiles. Bioresour. Technol. 184: 9-17. https://doi.org/10.1016/j.biortech.2014.11.003
  61. Shanmugam S, Mathimani T, Anto S, Sudhakar M, Kumar SS, Pugazhendhi A. 2020. Cell density, Lipidomic profile, and fatty acid characterization as selection criteria in bioprospecting of microalgae and cyanobacterium for biodiesel production. Bioresour. Technol. 304: 123061. https://doi.org/10.1016/j.biortech.2020.123061
  62. Patel VK, Sundaram S, Patel AK, Kalra A. 2018. Characterization of seven species of cyanobacteria for high-quality biomass production. Arab. J. Sci. Eng. 43: 109-121. https://doi.org/10.1007/s13369-017-2666-0
  63. Kings AJ, Raj RE, Miriam LM, Visvanathan MA. 2017. Cultivation, extraction and optimization of biodiesel production from potential microalgae Euglena sanguinea using eco-friendly natural catalyst. Energy Convers. Manag. 141: 224-235. https://doi.org/10.1016/j.enconman.2016.08.018
  64. Jacob-Lopes E, Santos AB, Severo IA, Depra MC, Maroneze MM, Zepka LQ. 2020. Dual production of bioenergy in heterotrophic cultures of cyanobacteria: Process performance, carbon balance, biofuel quality and sustainability metrics. Biomass Bioenergy 142: 105756. https://doi.org/10.1016/j.biombioe.2020.105756
  65. Dahiya S, Sarkar O, Swamy Y, Mohan SV. 2015. Acidogenic fermentation of food waste for volatile fatty acid production with cogeneration of biohydrogen. Bioresour. Technol. 182: 103-113. https://doi.org/10.1016/j.biortech.2015.01.007
  66. Esteban-Gutierrez M, Garcia-Aguirre J, Irizar I, Aymerich E. 2018. From sewage sludge and agri-food waste to VFA: Individual acid production potential and up-scaling. Waste Manage. 77: 203-212. https://doi.org/10.1016/j.wasman.2018.05.027
  67. Liu X, Liu H, Du G, Chen J. 2009. Improved bioconversion of volatile fatty acids from waste activated sludge by pretreatment. Water Environ. Res. 81: 13-20. https://doi.org/10.2175/106143008X304640
  68. Horiuchi J-I, Tabata K, Kanno T, Kobayashi M. 2000. Continuous acetic acid production by a packed bed bioreactor employing charcoal pellets derived from waste mushroom medium. J. Biosci. Bioeng. 89: 126-130. https://doi.org/10.1016/S1389-1723(00)88725-3
  69. Li Y, Su D, Feng H, Yan F, Liu H, Feng L, et al. 2017. Anaerobic acidogenic fermentation of food waste for mixed-acid production. Energy Sources A: Recovery Util. Environ. Eff. 39: 631-635.