Effects of light on cell growth, chlorophyll, and carotenoid contents of Chlorella sorokiniana and Ankistrodesmus falcatus in poultry dropping medium

Jane Chizie Ogbonna; Nkechinyere Onyekwere Nweze; Christiana Nwakego Ogbonna

doi:10.7324/JABB.2021.9215

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Abstract

Microalgae biomass and their products are invaluable bio-resources with numerous applications in food, feed, pharmacy, cosmetics, and environments. The effects of light intensities on biomass, chlorophyll-a, and total carotenoid production by Chlorella sorokiniana and Ankistrodesmus falcatus were studied in Bold’s Basal Medium (BBM) and Poultry Medium (PM) as the growth media. The growth of C. sorokiniana and A. falcatus increased with increase in light intensity in PM and was inhibited at 1786 lux in C. sorokiniana in BBM. PM supported higher biomass production by C. sorokiniana than BBM while it was the reverse for A. falcatus. A. falcatus produced higher (P ≤ 0.05) concentrations of chlorophyll-a than C. sorokiniana in both media. The highest carotenoid concentration of 11.84 mg/g-biomass was accumulated by C. sorokiniana in PM as against 7.027 mg/g-biomass obtained in BBM. On the other hand, the highest carotenoid concentration of 7.633 mg/g-biomass was accumulated by A. falcatus in BBM as against 4.299 mg/g-biomass obtained in PM. It is interesting to note in the present study that a cheap medium such as PM supported higher biomass and carotenoid production by C. sorokiniana than BBM.

Keyword: Microalgae Biomass Chlorella sorokiniana Ankistrodesmus falcatus Light intensity Chlorophyll Carotenoids.

Citation:

Ogbonna JC, Nweze NO, Ogbonna CN. Effects of light on cell growth, chlorophyll and carotenoid contents of Chlorella sorokiniana and Ankistrodesmus falcatus in poultry dropping medium. J App Biol Biotech. 2021;9(2):157-163.

Copyright: Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike license.

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Reference

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2. Schade S, Meier T. Distinct microalgae species for food-part 1: A methological (top-down) approach for the life cycle assessment of microalgae cultivation in tubular photobioreactors. J Appl Phycol 2020;32:2977-95. https://doi.org/10.1007/s10811-020-02177-2
3. Schade S, Stangl GI, Meier T. Distinct microalgae species for foodpart 2: Comparative life cycle assessment of microalgae and fish for eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and protein. J Appl Phycol 2020;32:2997-3013. https://doi.org/10.1007/s10811-020-02181-6
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5. Cordero BF, Obraztsova I, Couso I, Leon R, Vargas MA, Rodriguez H. Enhancement of lutein production in Chlorella sorokiniana (Chlorophyta) by improvement of culture conditions and random mutagenesis. Mar Drugs 2011;9:1607-24. https://doi.org/10.3390/md9091607
6. Novoveska L, Ross ME, Stanley MS, Pradelles R, Wasiolek V, Sassi JF. Microalgal carotenoids: A review of production, current markets, regulations and future direction. Mar Drugs 2019;17:640. https://doi.org/10.3390/md17110640
7. Nwoba EG, Ogbonna CN, Ishika T, Vadiveloo A. Microalgal pigments: A source of natural food colors In: Alam A, Xu JL, Wang Z, editors. Microalgae Biotechnology for Food, Health and High Value Products. Germany: Springer; 2020. p. 81-123. https://doi.org/10.1007/978-981-15-0169-2_3
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9. Amin M, Chetpattananond P, Khan MN, Mushtaq F, Sami SK. Extraction and quantification of chlorophyll from microalgae Chlorella sp. IOP Conf Ser Mater Sci Eng 2018;414:012025. https://doi.org/10.1088/1757-899X/414/1/012025
10. Sangapillai K, Marimuthu T. Isolation and selection of growth medium for fresh water microalgae Asterarcys quadricellulare for maximum biomass production. Water Sci Technol 2019;80:2027-36. https://doi.org/10.2166/wst.2020.015
11. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, et al. Algae as nutritional and functional food sources: Revisiting our understanding. J Appl Phycol 2017;29:949-82. https://doi.org/10.1007/s10811-016-0974-5
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21. Fulke A, Chakrabarti T, Kannan K, Sivanesan S. CO2 Sequestration by microalgae: Advances and perspectives. In: Liu J, Sun Z, Gerken H, editors. Recent Advances and Perspectives. United States: OMICS Group Incorporation; 2014. p. 1-7.
22. Pourjamshidian R, Abolghasermi H, Esmaili M, Amrei HD, Parsa M, Rezaei S. Carbon dioxide biofixation by Chlorella sp. In a bubble column reactor at different flow rates and CO2 concentrations. Braz J Chem Eng 2019;36:639-45. https://doi.org/10.1590/0104-6632.20190362s20180151
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24. Ferruzi MG, Bohn V, Courtney PD, Schwartz SJ. Antioxidant and antimutagenic activity of dietary chlorophyll derivatives determined by radical scavenging and bacterial reverse mutagenesis assays. J Food Sci 2006;67:2589-95. https://doi.org/10.1111/j.1365-2621.2002.tb08782.x
25. Ferreira VS, Sant'Anna C. Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World J Microbiol Biotechnol 2016;33:20. https://doi.org/10.1007/s11274-016-2181-6
26. Sarkar S, Manna MS, Bhowmick TK, Gayen K. Extraction of chlorophyll and carotenoids from dry and wet biomass of isolated Chlorella thermophila: Optimization of process parameters and modelling by artificial neural network. Process Biochem 2020;96:58-72. https://doi.org/10.1016/j.procbio.2020.05.025
27. Singh DP, Khattar JS, Rajput A, Chaudhary R, Singh R. High production of carotenoids by the green microalga Asterarcys quadricellulare PUMCC 5.1.1 under optimized culture conditions. PLoS One 2019;14:e0221930. https://doi.org/10.1371/journal.pone.0221930
28. Ogbonna CN. Production of food colourant by Filamentous fungi. Afr J Microbiol Res 2016;10:960-71. https://doi.org/10.5897/AJMR2016.7904
29. Ogbonna CN, Aoyagi H, Ogbonna JC. Isolation and identification of Talaromyces purpuorogenus and preliminary studies on its pigment production in solid state cultures. Afr J Biotechnol 2017;16:672-82. https://doi.org/10.5897/AJB2016.15798
30. Ambati RR, Gogisetty D, Aswathanarayana RG, Ravi S, Bikkina PN, Bo L, et al. Industrial potential of carotenoid pigments from microalgae: Current trends and future prospects. Crit Rev Food Sci Nutr 2017;59:1880-902. https://doi.org/10.1080/10408398.2018.1432561
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33. Sibi G. Low cost carbon and nitrogen sources for high microalgal biomass and lipid production using agricultural wastes. J Environ Sci Technol 2015;8:113-21. https://doi.org/10.3923/jest.2015.113.121
34. Rogeri DA, Ernani PR, Mantovani A, Lourenco KS. Composition of poultry litter in Southern Brazil. Rev Bras Cienc 2016;40:e0140697. https://doi.org/10.1590/18069657rbcs20140697
35. Ogbonna JC, Yada H, Tanaka H. Kinetic study on light limited batch cultivation of photo synthetic cells. J Fermen Bioeng 1995;80:259-64. https://doi.org/10.1016/0922-338X(95)90826-L
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42. Kumar V, Kumar A, Nanda M. Pretreated animal and human waste as a substantial nutrient source for cultivation of microalgae for biodiesel production. Environ Sci Pollut Res 2018;25:22052-9. https://doi.org/10.1007/s11356-018-2339-x
43. Wang Y, Liu S, Tian X, Fu Y, Jiang X, Li Y. Influence of light intensity on chloroplast development and pigment accumulation in the wild-type and etiolated mutant plants of Anthurium andraeanum Sonate. Plant Signal Behav 2018;13:e1482174. https://doi.org/10.1080/15592324.2018.1482174
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1. Hernandez D, Molinuevo-Salces B, Riano B, Larran-Garcia AM, Tomas-Almenar CT, Garcia-Gonzalez MC. Recovery of protein concentrates from microalgal biomass grown in manure for fish feed and valorization of the by-products through anaerobic digestion. Front Sustain Food Syst 2018;2:28. https://doi.org/10.3389/fsufs.2018.00028

2. Schade S, Meier T. Distinct microalgae species for food-part 1: A methological (top-down) approach for the life cycle assessment of microalgae cultivation in tubular photobioreactors. J Appl Phycol 2020;32:2977-95. https://doi.org/10.1007/s10811-020-02177-2

3. Schade S, Stangl GI, Meier T. Distinct microalgae species for foodpart 2: Comparative life cycle assessment of microalgae and fish for eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and protein. J Appl Phycol 2020;32:2997-3013. https://doi.org/10.1007/s10811-020-02181-6

4. Cheng D, Li D, Yuan Y, Zhou L, Li X, Wu T, et al. Improving carbohydrate and starch accumulation in Chlorella sp. AE10 by a novel two-stage process with cell dilution. Biotechnol Biofuels 2017;10:75. https://doi.org/10.1186/s13068-017-0753-9

5. Cordero BF, Obraztsova I, Couso I, Leon R, Vargas MA, Rodriguez H. Enhancement of lutein production in Chlorella sorokiniana (Chlorophyta) by improvement of culture conditions and random mutagenesis. Mar Drugs 2011;9:1607-24. https://doi.org/10.3390/md9091607

6. Novoveska L, Ross ME, Stanley MS, Pradelles R, Wasiolek V, Sassi JF. Microalgal carotenoids: A review of production, current markets, regulations and future direction. Mar Drugs 2019;17:640. https://doi.org/10.3390/md17110640

7. Nwoba EG, Ogbonna CN, Ishika T, Vadiveloo A. Microalgal pigments: A source of natural food colors In: Alam A, Xu JL, Wang Z, editors. Microalgae Biotechnology for Food, Health and High Value Products. Germany: Springer; 2020. p. 81-123. https://doi.org/10.1007/978-981-15-0169-2_3

8. Ogbonna IO, Ogbonna JC. Isolation of microalgae species from arid environments and evaluation of their potentials for biodiesel production. Afr J Biotechnol 2015;14:1596-604. https://doi.org/10.5897/AJB2014.14327

9. Amin M, Chetpattananond P, Khan MN, Mushtaq F, Sami SK. Extraction and quantification of chlorophyll from microalgae Chlorella sp. IOP Conf Ser Mater Sci Eng 2018;414:012025. https://doi.org/10.1088/1757-899X/414/1/012025

10. Sangapillai K, Marimuthu T. Isolation and selection of growth medium for fresh water microalgae Asterarcys quadricellulare for maximum biomass production. Water Sci Technol 2019;80:2027-36. https://doi.org/10.2166/wst.2020.015

11. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, et al. Algae as nutritional and functional food sources: Revisiting our understanding. J Appl Phycol 2017;29:949-82. https://doi.org/10.1007/s10811-016-0974-5

12. Keller H, Reinhardt GA, Rettenmaier N, Schrb A, Dittrch M. Environmenat assessment of algae-based polyunsaturated fatty acid PUFA. In: PUFA Chain Project Reports, Supported by the EU's FP7 Under GA No. 613307. Heidelberg, Germany: IFEU-Institute of Energy and Environmental Research Heidelberg; 2017.

13. Borowitzka M. Commercial-scale production of microalgae for bioproducts. In: La barre S, Bates S, editors. Blue Biotechnology: Production and Use of Marine Molecules. Weinheim: Wiley-VCH; 2018. p. 33-65. https://doi.org/10.1002/9783527801718.ch2

14. Khan MI, Shin JH, Kim JD. The promising future f microalgae: Current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Factories 2018;17:36.htt ps://doi.org/10.1186/s12934-018-0879-x

15. Aratboni HA, Rafiei N, Garcia-Granados R, Alemzadeh A, MoronesRamirez JR. Biomass and lipid induction strategies in microalgae for biofuel production and other applications. Microb Cell Factories 2019;18:178. https://doi.org/10.1186/s12934-019-1228-4

16. Sayre R. Microalgae: The potential for carbon capture. Bio Sci 2010;60:722-7. https://doi.org/10.1525/bio.2010.60.9.9

17. Begum H, Yusoff FM, Bannerjee S, Khatoon H, Shariff M. Availability and utilization of pigments from microalgae. Crit Rev Food Sci Nutr 2015;56:2209-22. https://doi.org/10.1080/10408398.2013.764841

18. Cezare-Gomes EA, Mejia-da-Silva LC, Perez-Mora LS, Matsudo MC, Ferreira-Camargo LS. Potential of microalgae carotenoids for industrial application. Appl Biochem Biotechnol 2019;188:602-34. https://doi.org/10.1007/s12010-018-02945-4

19. Vadiveloo A, Nwoba EG, Ogbonna C, Mehta P. Sustainable production of bioproducts from wastewater-grown microalgae. In: Gayen K, Bhowmick TK, Maity SK, editors. Sustainable Downstream Processing of Microalgae for Industrial Application. United Kingdom: CRC Press, Taylor and Francis; 2019. p. 165-200. https://doi.org/10.1201/9780429027970-7

20. Nwoba EG, Vadiveloo AA, Ogbonna CN, Ubi BE, Ogbonna JC, Moheimani NR. Algal cultivation for treating wastewater in African developing countries. A review. Clean (Weinh) 2020;48:2000052. https://doi.org/10.1002/clen.202000052

21. Fulke A, Chakrabarti T, Kannan K, Sivanesan S. CO2 Sequestration by microalgae: Advances and perspectives. In: Liu J, Sun Z, Gerken H, editors. Recent Advances and Perspectives. United States: OMICS Group Incorporation; 2014. p. 1-7.

22. Pourjamshidian R, Abolghasermi H, Esmaili M, Amrei HD, Parsa M, Rezaei S. Carbon dioxide biofixation by Chlorella sp. In a bubble column reactor at different flow rates and CO2 concentrations. Braz J Chem Eng 2019;36:639-45. https://doi.org/10.1590/0104-6632.20190362s20180151

23. Ong TM, Whong WZ, Stewart J, Brockman HE. Chlorophyllin: A potent antimutagen against environmental and dietary complex mixtures. Mutat Res 1986;173:111. https://doi.org/10.1016/0165-7992(86)90086-2

24. Ferruzi MG, Bohn V, Courtney PD, Schwartz SJ. Antioxidant and antimutagenic activity of dietary chlorophyll derivatives determined by radical scavenging and bacterial reverse mutagenesis assays. J Food Sci 2006;67:2589-95. https://doi.org/10.1111/j.1365-2621.2002.tb08782.x

25. Ferreira VS, Sant'Anna C. Impact of culture conditions on the chlorophyll content of microalgae for biotechnological applications. World J Microbiol Biotechnol 2016;33:20. https://doi.org/10.1007/s11274-016-2181-6

26. Sarkar S, Manna MS, Bhowmick TK, Gayen K. Extraction of chlorophyll and carotenoids from dry and wet biomass of isolated Chlorella thermophila: Optimization of process parameters and modelling by artificial neural network. Process Biochem 2020;96:58-72. https://doi.org/10.1016/j.procbio.2020.05.025

27. Singh DP, Khattar JS, Rajput A, Chaudhary R, Singh R. High production of carotenoids by the green microalga Asterarcys quadricellulare PUMCC 5.1.1 under optimized culture conditions. PLoS One 2019;14:e0221930. https://doi.org/10.1371/journal.pone.0221930

28. Ogbonna CN. Production of food colourant by Filamentous fungi. Afr J Microbiol Res 2016;10:960-71. https://doi.org/10.5897/AJMR2016.7904

29. Ogbonna CN, Aoyagi H, Ogbonna JC. Isolation and identification of Talaromyces purpuorogenus and preliminary studies on its pigment production in solid state cultures. Afr J Biotechnol 2017;16:672-82. https://doi.org/10.5897/AJB2016.15798

30. Ambati RR, Gogisetty D, Aswathanarayana RG, Ravi S, Bikkina PN, Bo L, et al. Industrial potential of carotenoid pigments from microalgae: Current trends and future prospects. Crit Rev Food Sci Nutr 2017;59:1880-902. https://doi.org/10.1080/10408398.2018.1432561

31. Available from: https://www.marketsandmarkets.com/Market-Reports/ carotenoid-market-158421566.html. [Last accessed on 2020 Aug 05].

32. Singh M, Das KC. Low cost nutrients for algae cultivation. In: Bajpai R, Prokop A, Zappi M, editors. Starch Overproduction by Means of Algae. Netherlands: Springer; 2014. p. 69-82. https://doi.org/10.1007/978-94-007-7494-0_3

33. Sibi G. Low cost carbon and nitrogen sources for high microalgal biomass and lipid production using agricultural wastes. J Environ Sci Technol 2015;8:113-21. https://doi.org/10.3923/jest.2015.113.121

34. Rogeri DA, Ernani PR, Mantovani A, Lourenco KS. Composition of poultry litter in Southern Brazil. Rev Bras Cienc 2016;40:e0140697. https://doi.org/10.1590/18069657rbcs20140697

35. Ogbonna JC, Yada H, Tanaka H. Kinetic study on light limited batch cultivation of photo synthetic cells. J Fermen Bioeng 1995;80:259-64. https://doi.org/10.1016/0922-338X(95)90826-L

36. Matos AP, Ferreira WB, Morioka LR, Moecke EH, Franca KB, Sant' Anna ES. Cultivation of Chlorella vulgaris in medium supplemented with desalination concentrate grown in a pilot-scale open raceway. Braz J Chem Eng 2018;35:1183-92. https://doi.org/10.1590/0104-6632.20180354s20170338

37. Markou G, Iconomou D, Muylaert K. Applying raw poultry liter leachate for the cultivation of Arthrospira platensis and Chlorella vulgaris. Algal Res 2016;13:79-84. https://doi.org/10.1016/j.algal.2015.11.018

38. Becker EW. Microalgae: Biotechnology and Microbiology. United Kingdom: Cambridge University Press; 1994. p. 293.

39. Branisa J, Jenisova Z, Porubska M, Jomova K. Spectrophotometric determination of chlorophylls and carotenoids. An effect of sonication and sample processing. J Microbiol Biotech Food Sci 2014;3:61-4.

40. Metsoviti MN, Pappoolymerou G, Karapanagiotidis IT, Katsoulas N. Effect of light intensity and quality on growth of Chlorella vulgaris. Plants Basel 2020;9:31. https://doi.org/10.3390/plants9010031

41. Nzayisenga JC, Farge X, Goll SL, Sellstedt A. Effects of light intensity on growth and lipid production in microalgae grown in wastewater. Biotechnol Biofuels 2020;13:4. https://doi.org/10.1186/s13068-019-1646-x

42. Kumar V, Kumar A, Nanda M. Pretreated animal and human waste as a substantial nutrient source for cultivation of microalgae for biodiesel production. Environ Sci Pollut Res 2018;25:22052-9. https://doi.org/10.1007/s11356-018-2339-x

43. Wang Y, Liu S, Tian X, Fu Y, Jiang X, Li Y. Influence of light intensity on chloroplast development and pigment accumulation in the wild-type and etiolated mutant plants of Anthurium andraeanum Sonate. Plant Signal Behav 2018;13:e1482174. https://doi.org/10.1080/15592324.2018.1482174

44. Kang D, Kim KT, Heo TY, Kwon G, Lim C, Park J. Inhibition of photosynthetic activity in wastewater-borne microalgal-bacterial consortia under various light conditions. Sustainability 2019;11:2951. https://doi.org/10.3390/su11102951

45. Jalal KC, Shamsuddin AA, Rahman MF, Nurzatul NZ, Rozihan M. Growth and total carotenoid, chlorophyll a and chlorophyll b of tropical microalgae (Isochrysis sp.) in laboratory cultured conditions. J Biol Sci 2019;13:10-7. https://doi.org/10.3923/jbs.2013.10.17

46. Raman R, Mohamad SE. Astaxanthin production by freshwater microalgae Chlorella sorokiniana and marine microalgae Tetraselmis sp. Pak J Biol Sci 2013;15:1182-6. https://doi.org/10.3923/pjbs.2012.1182.1186

47. Iyovo DV, Guocheng D, Jian C. Poultry manure digestate enhancement of Chlorella vulgaris biomass under mixotrophic condition for biofuel production. J Microb Biochem Technol 2010;2:1000023.

48. Agwa OK, Abu GO. Utilization of poultry waste for the cultivation of Chlorella sp. for biomass and lipid production. Int J Curr Microbiol Appl Sci 2014;3:1036-47.

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