Abstract
The microalgae industry shows a promising future in the production of high-value products such as pigments, phycoerythrin, polyunsaturated fatty acids, and polysaccharides. It was found that polysaccharides have high biomedical value (such as antiviral, antibacterial, antitumor, antioxidative) and industrial application prospects (such as antioxidants). This study aimed to improve the polysaccharides accumulation of Porphyridium purpureum CoE1, which was effectuated by inorganic salt starvation strategy whilst supplying rich carbon dioxide. At a culturing temperature of 25 °C, the highest polysaccharide content (2.89 g/L) was achieved in 50% artificial seawater on the 12th day. This accounted for approximately 37.29% of the dry biomass, signifying a 25.3% increase in polysaccharide production compared to the culture in 100% artificial seawater. Subsequently, separation, purification and characterization of polysaccharides produced were conducted. Furthermore, the assessment of CO2 fixation capacity during the cultivation of P. purpureum CoE1 was conducted in a 10 L photobioreactor. This indicated that the strain exhibited an excellent CO2 fixation capacity of 1.66 g CO2/g biomass/d. This study proposed an efficient and feasible approach that not only increasing the yield of polysaccharides by P. purpureum CoE1, but also fixing CO2 with a high rate, which showed great potential in the microalgae industry and Bio-Energy with Carbon Capture and Storage.
Similar content being viewed by others
References
Wang X, Wang X, Jiang H, Cai C, Li G, Hao J, Yu G (2018) Marine polysaccharides attenuate metabolic syndrome by fermentation products and altering gut microbiota: an overview. Carbohydr Polym 195:601–612. https://doi.org/10.1016/j.carbpol.2018.05.003
Zhang L, Hu Y, Duan X, Tang T, Shen Y, Hu B, Liu A, Chen H, Li C, Liu Y (2018) Characterization and antioxidant activities of polysaccharides from thirteen boletus mushrooms. Int J Biol Macromol 113:1–7. https://doi.org/10.1016/j.ijbiomac.2018.02.084
Delattre C, Pierre G, Laroche C, Michaud P (2016) Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnol Adv 34:1159–1179. https://doi.org/10.1016/j.biotechadv.2016.08.001
Wang Z, Wen X, Xu Y, Ding Y, Geng Y, Li Y (2018) Maximizing CO2 biofixation and lipid productivity of oleaginous microalga Graesiella sp. WBG-1 via CO2-regulated pH in indoor and outdoor open reactors. Sci Total Environ 619:827–833. https://doi.org/10.1016/j.scitotenv.2017.10.127
Jiao K, Chang J, Zeng X, Ng I-S, Xiao Z, Sun Y, Tang X, Lin L (2017) 5-Aminolevulinic acid promotes arachidonic acid biosynthesis in the red microalga Porphyridium purpureum. Biotechnol Biofuels 10:168. https://doi.org/10.1186/s13068-017-0855-4
Xu Y, Jiao K, Zhong H, Wu S, Ho SH, Zeng X, Li J, Tang X, Sun Y, Lin L (2020) Correction to: Induced cultivation pattern enhanced the phycoerythrin production in red alga Porphyridium purpureum. Bioprocess Biosyst Eng 43:357. https://doi.org/10.1007/s00449-019-02274-8
Su G, Jiao K, Chang J, Li Z, Guo X, Sun Y, Zeng X, Lu Y, Lin L (2016) Enhancing total fatty acids and arachidonic acid production by the red microalgae Porphyridium purpureum. Bioresour Bioprocess 3:33. https://doi.org/10.1186/s40643-016-0110-z
Chang J, Le K, Song X, Jiao K, Zeng X, Ling X, Shi T, Tang X, Sun Y, Lin L (2017) Scale-up cultivation enhanced arachidonic acid accumulation by red microalgae Porphyridium purpureum. Bioprocess Biosyst Eng 40:1763–1773. https://doi.org/10.1007/s00449-017-1831-x
Jiao K, Xiao W, Xu Y, Zeng X, Ho SH, Laws EA, Lu Y, Ling X, Shi T, Sun Y, Tang X, Lin L (2018) Using a trait-based approach to optimize mixotrophic growth of the red microalga Porphyridium purpureum towards fatty acid production. Biotechnol Biofuels 11:273. https://doi.org/10.1186/s13068-018-1277-7
Chen L, Huang G (2018) The antiviral activity of polysaccharides and their derivatives. Int J Biol Macromol 115:77–82. https://doi.org/10.1016/j.ijbiomac.2018.04.056
Netanel Liberman G, Ochbaum G, Malis Arad S, Bitton R (2016) The sulfated polysaccharide from a marine red microalga as a platform for the incorporation of zinc ions. Carbohydr Polym 152:658–664. https://doi.org/10.1016/j.carbpol.2016.07.025
Zhong Q, Wei B, Wang S, Ke S, Chen J, Zhang H, Wang H (2019) The antioxidant activity of polysaccharides derived from marine organisms: an overview. Mar Drugs 17:674. https://doi.org/10.3390/md17120674
Sutherland IW (2007) Bacterial exopolysaccharides. Compr Glycosci 2:521–558. https://doi.org/10.1016/B978-044451967-2/00133-1
Kumar K, Dasgupta CN, Nayak B, Lindblad P, Das D (2011) Development of suitable photobioreactors for CO2 sequestration addressing global warming using green algae and cyanobacteria. Bioresour Technol 102:4945–4953. https://doi.org/10.1016/j.biortech.2011.01.054
Iqbal M, Zafar SI (1993) Effects of photon flux density, CO2, aeration rate, and inoculum density on growth and extracellular polysaccharide production by Porphyridium cruentum. Folia Microbiol 38:509–514. https://doi.org/10.1007/BF02814405
Soanen N, Silva ED, Gardarin C, Michaud P, Laroche C (2016) Improvement of exopolysaccharide production by Porphyridium marinum. Bioresour Technol 213:231–238. https://doi.org/10.1016/j.biortech.2016.02.075
Cuellar-Bermudez SP, Aguilar-Hernandez I, Cardenas-Chavez DL, Ornelas-Soto N, Romero-Ogawa MA, Parra-Saldivar R (2015) Extraction and purification of high-value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microb Biotechnol 8:190–209. https://doi.org/10.1111/1751-7915.12167
Sun L, Wang C, Ma C, Shi L (2010) Optimization of renewal regime for improvement of polysaccharides production from Porphyridium cruentum by uniform design. Bioprocess Biosyst Eng 33:309–315. https://doi.org/10.1007/s00449-009-0325-x
Li S, Ji L, Chen C, Zhao S, Sun M, Gao Z, Wu H, Fan J (2020) Efficient accumulation of high-value bioactive substances by carbon to nitrogen ratio regulation in marine microalgae Porphyridium purpureum. Bioresour Technol 309:123362. https://doi.org/10.1016/j.biortech.2020.123362
Jiao K, Xiao W, Shi X, Ho SH, Chang JS, Ng IS, Tang X, Sun Y, Zeng X, Lin L (2021) Molecular mechanism of arachidonic acid biosynthesis in Porphyridium purpureum promoted by nitrogen limitation. Bioprocess Biosyst Eng 44:1491–1499. https://doi.org/10.1007/s00449-021-02533-7
Chopin T, Yarish C, Wilkes R, Belyea E, Lu S, Mathieson A (2000) Developing Porphyra/salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. J Appl Phycol 12:99. https://doi.org/10.1023/A:1008189312167
Beer S, Eshel A (1985) Determining phycoerythrin and phycocyanin concentrations in aqueous crude extracts of red algae. Mar Freshwater Res 36:785–792. https://doi.org/10.1071/MF9850785
Coward T, Fuentes-Grünewald C, Silkina A, Oatley-Radcliffe DL, Llewellyn G, Lovitt RW (2016) Utilising light-emitting diodes of specific narrow wavelengths for the optimization and co-production of multiple high-value compounds in Porphyridium purpureum. Bioresour Technol 221:607–615. https://doi.org/10.1016/j.biortech.2016.09.093
Li Q, Chen Y, Liu X, Li Y, Xu J, Li T, Xiang W, Li A (2023) Effect of salinity on the biochemical characteristics and antioxidant activity of exopolysaccharide of Porphyridium purpureum FACHB 806. Front Mar Sci 9:1097200. https://doi.org/10.3389/fmars.2022.1097200
Fimbres-Olivarria D, Carvajal-Millan E, Lopez-Elias JA, Martinez-Robinson KG, Miranda-Baeza A, Martinez-Cordova LR, Enriquez-Ocaa F, Valdez-Holguin JE (2018) Chemical characterization and antioxidant activity of sulfated polysaccharides from Navicula sp. Food Hydrocolloids 75:229–236. https://doi.org/10.1016/j.foodhyd.2017.08.002
Shahid A, Malik S, Zhu H, Xu J, Nawaz MZ, Nawaz S, Alam MA, Mehmood MA (2019) Cultivating microalgae in wastewater for biomass production, pollutant removal, and atmospheric carbon mitigation; a review. Sci Total Environ 704:135303. https://doi.org/10.1016/j.scitotenv.2019.135303
Nair AT, Senthilnathan J, Nagendra SMS (2019) Application of the phycoremediation process for tertiary treatment of landfill leachate and carbon dioxide mitigation. J Water Process Eng 28:322–330. https://doi.org/10.1016/j.jwpe.2019.02.017
Iqbal M, Grey D, Sepan-Sarkissian G, Fowler MW (1993) Interactions between the unicellular red alga Porphyridium cruentum and associated bacteria. EUR J PHYCOL 28:63–68. https://doi.org/10.1080/09670269300650101
Iqbal M, Zafar SI (1993) Bioactivity of immobilized microalgal cells: application potential of vegetable sponge in microbial biotechnology. Lett Appl Microbiol 17:289–291. https://doi.org/10.1111/j.1472-765x.1993.tb01469.x
Wang J, Chen B, Rao X, Huang J, Li M (2007) Optimization of culturing conditions of Porphyridium cruentum using uniform design. World J Microbiol Biotechnol 23:1345–1350. https://doi.org/10.1007/s11274-007-9369-8
Lu X, Nan F, Feng J, Lv J, Liu Q, Liu X, Xie S (2020) Effects of different environmental factors on the growth and bioactive substance accumulation of Porphyridium purpureum. Int J Environ Res Public Health 17:2221. https://doi.org/10.3390/ijerph17072221
Ji L, Li S, Chen C, Jin H, Wu H, Fan J (2021) Physiological and transcriptome analysis elucidates the metabolic mechanism of versatile Porphyridium purpureum under nitrogen deprivation for exopolysaccharides accumulation. Bioresour Bioprocess 8:73. https://doi.org/10.1186/s40643-021-00426-x
Ferreira AS, Mendonça I, Póvoa I, Carvalho H, Correia A, Vilanova M, Silva TH, Coimbra MA, Nunes C (2021) Impact of growth medium salinity on galactoxylan exopolysaccharides of Porphyridium purpureum. Algal Res 59:102439. https://doi.org/10.1016/j.algal.2021.102439
Parra-Riofrío G, Casas-Arrojo V, Pino-Selles R, García-Márquez J, Abdala-Díaz RT, Uribe-Tapia E (2021) Adaptation of autotrophic to heterotrophic culture of Porphyridium purpureum (Bory) K.M. Drew & R. Ross: characterization of biomass and production of exopolysaccharides. J Appl Phycol 33:3603–3615. https://doi.org/10.1007/s10811-021-02566-1
Zhang AH, Feng B, Zhang H, Jiang J, Zhang D, Du Y, Cheng Z, Huang J (2022) Efficient cultivation of Porphyridium purpureum integrated with swine wastewater treatment to produce phycoerythrin and polysaccharide. J Appl Phycol 34:2315–2326. https://doi.org/10.1007/s10811-022-02785-0
Yin H-C, Sui J-K, Han T-L, Liu T-Z, Wang H (2022) Integration bioprocess of B-phycoerythrin and exopolysaccharides production from photosynthetic microalga Porphyridium cruentum. Front Mar Sci 8:836370. https://doi.org/10.3389/fmars.2021.836370
Lv JM, Cheng LH, Xu XH, Zhang L, Chen HL (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101:6797–6804. https://doi.org/10.1016/j.biortech.2010.03.120
Recht L, Zarka A, Boussiba S (2012) Patterns of carbohydrate and fatty acid changes under nitrogen starvation in the microalgae Haematococcus pluvialis and Nannochloropsis sp. Appl Microbiol Biot 94:1495–1503. https://doi.org/10.1007/s00253-012-3940-4
Sheath RG, Hellebust JA, Sawa T (1979) Floridean starch metabolism of Porphyridium purpureum (Rhodophyta). II. Changes during the cell cycle*. Phycologia 18:185–190. https://doi.org/10.2216/i0031-8884-18-3-185.1
Biller P, Ross AB, Skill SC, Lea-Langton A, Balasundaram B, Hall C, Riley R, Llewellyn CA (2012) Nutrient recycling of aqueous phase for microalgae cultivation from the hydrothermal liquefaction process. Algal Res 1:70–76. https://doi.org/10.1016/j.algal.2012.02.002
Khan MI, Shin JH, Kim JD (2018) The promising future of microalgae: current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb Cell Fact 17:36. https://doi.org/10.1186/s12934-018-0879-x
Schoeters F, Spit J, Swinnen E, Cuyper AD, Vleugels R, Miert INSV (2023) Pilot-scale cultivation of the red alga Porphyridium purpureum over a two-year period in a greenhouse. J Appl Phycol 35:2095–2109. https://doi.org/10.1007/s10811-023-03045-5
Akimoto M, Shirai A, Ohtaguchi K, Koide K (1998) Carbon dioxide fixation and polyunsaturated fatty acid production by the red alga porphyridium cruentum. Appl Biochem Biotech 73:269–278. https://doi.org/10.1007/BF02785661
Acknowledgements
This work was financially supported by the special fund for Fujian Ocean High-Tech Industry Development (No. FJHJF-L-2018-1) and the Natural Science Foundation of Fujian Province of China (No. 2019J06005).
Author information
Authors and Affiliations
Contributions
LY and WS carried out the experiments and data analysis. LY, WS, CH, XW, LC, PZ, LZ, LJ and ZX wrote the manuscript. WS and ZX revised the manuscript. WS, XW, LL and ZX contributed to resource and methodology. ZX managed and supervised the project. All the authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Data availability
The authors declare that the data supporting the findings in this study are presented within the paper. The data are also available from the corresponding author upon request.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, Y., Wu, S., Chen, H. et al. Inorganic salt starvation improves the polysaccharide production and CO2 fixation by Porphyridium purpureum. Bioprocess Biosyst Eng (2024). https://doi.org/10.1007/s00449-024-03017-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00449-024-03017-0