Abstract
The aerial microalga (Coccomyxa subellipsoidea KGU-D001) was photoautotrophically cultured under aerial phase conditions, and the influence of the nitrogen source on lipid production was investigated. Coccomyxa biofilms were introduced onto cotton wool using pure water (i.e., nutrient depletion) or a nitrogen-containing solution in a Petri dish, and they were cultured for 14 days under aerial phase conditions. The biomass in the biofilm increased by more than 150% in 14 days under nutrient depleted conditions and then increased further by approximately 30% following the addition of a nitrogen source. The lipid content rose under both nutrient depletion and nitrogen-added conditions, increasing by 170 and 150% in 14 days, respectively. The protein and sugar contents were also monitored and analyzed. In the presence of a nitrogen source, C. subellipsoidea undergo cell division in a relatively short time span, and biomass and lipids can be synthesized under both nutrient depleted and nitrogen-added conditions.
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The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.
References
Abe K, Bito T, Sato A, Aburai N (2014a) Effects of light intensity and magnesium supplementation in pretreatment cycle on ammonium removal from wastewater of photobioreactor using a biofilter composed of the aerial microalga Trentepohlia aurea. J Appl Phycol 26:341–347. https://doi.org/10.1007/s12010-014-1181-y
Abe K, Ishiwatari T, Wakamatsu M, Aburai N (2014b) Fatty acid content and profile of the aerial microalga Coccomyxa sp. isolated from dry environments. Appl Biochem Biotechnol 174:1724–1735. https://doi.org/10.1007/s10811-013-0106-4
Aburai N, Maruyama S, Shimizu K, Abe K (2019) Production of bioactive oligopeptide hydrolyzed by protease derived from aerial microalga Vischeria helvetica. J Biotechnol 294:67–72. https://doi.org/10.1016/j.jbiotec.2019.01.021
Aburai N, Nishida A, Abe K (2021) Aerial microalgae Coccomyxa simplex isolated from a low-temperature, low-light environment, and its biofilm growth and lipid accumulation. Algal Res 60:102522. https://doi.org/10.1016/j.algal.2021.102522
Acton E (1909) Coccomyxa subellipsoidea, a new member of the Palmellaceae. Ann Bot 23:573–578. https://doi.org/10.1093/oxfordjournals.aob.a089239
Ananthi V, Brindhadevi K, Pugazhendhi A, Arun A (2021) Impact of abiotic factors on biodiesel production by microalgae. Fuel 284:118962. https://doi.org/10.1016/j.fuel.2020.118962
Cheng Y-S, Labavitch JM, VanderGheynst JS (2014) Elevated CO2 concentration impacts cell wall polysaccharide composition of green microalgae of the genus Chlorella. Lett Appl Microbiol 60:1–7. https://doi.org/10.1111/lam.12320
Danesh AF, Ebrahimi S, Salehi A, Parsa A (2017) Impact of nutrient starvation on intracellular biochemicals and calorific value of mixed microalgae. Biochem Eng J 125:56–64. https://doi.org/10.1016/j.bej.2017.05.017
Gojkovic Z, Lu Y, Ferro L, Toffolo A, Funk C (2020) Modeling biomass production during progressive nitrogen starvation by North Swedish green microalgae. Algal Res 47:101835. https://doi.org/10.1016/j.algal.2020.101835
González-Hourcade M, del Campo EM, Casano LM (2021) The under-explored extracellular proteome of aero-terrestrial microalgae provides clues on different mechanisms of desiccation tolerance in non-model organisms. Microb Ecol 81:437–453. https://doi.org/10.1007/s00248-020-01604-8
Iverson SJ, Lang SLC, Cooper MH (2001) Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 36:1283–1287. https://doi.org/10.1007/s11745-001-0843-0
Maltsev Y, Maltseva I, Maltseva S, Kociolek J, Kulikovskiy M (2019) Fatty acid content and profile of the novel strain of Coccomyxa elongata (Trebouxiophyceae, Chlorophyta) cultivated at reduced nitrogen and phosphorus concentrations. J Phycol 55:1154–1165. https://doi.org/10.1111/jpy.12903
Mantzorou A, Ververidis F (2019) Microalgal biofilms: a further step over current microalgal cultivation techniques. Sci Total Environ 651:3187–3201. https://doi.org/10.1016/j.scitotenv.2018.09.355
Miyauchi H, Okada K, Fujiwara S, Tsuzuki M (2020) Characterization of CO2 fixation on algal biofilms with an infrared gas analyzer and importance of a space-rich structure on the surface. Algal Res 46:101814. https://doi.org/10.1016/j.algal.2020.101814
Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75:50–59. https://doi.org/10.1016/j.phytochem.2011.12.007
Nicolò MS, Gugliandolo C, Rizzo MG, Zammuto V, Cicero N, Dugo G, Pietro S, Guglielmino P (2021) Nutritional conditions of the novel freshwater Coccomyxa AP01 for versatile fatty acids composition. J Appl Microbiol 00:1–12. https://doi.org/10.1111/jam.15223
Ohkubo K, Aburai N, Miyashita H, Tsuzuki M, Abe K (2017) CO2 fixation and lipid accumulation in biofilms of the aerial microalga Coccomyxa sp. KGU-D001 (Trebouxiophyceae). J Appl Phycol 29:1745–1753. https://doi.org/10.1007/s10811-017-1123-5
Palmqvist K, Sültemeyer D, Baldet P, Andrews TJ, Badger MR (1995) Characterisation of inorganic carbon fluxes, carbonic anhydrase(s) and ribulose-1,5-biphosphate carboxylase-oxygenase in the green unicellular alga Coccomyxa. Planta 197:352–361. https://doi.org/10.1007/BF00202657
Peng H, Wei D, Chen G, Chen F (2016) Transcriptome analysis reveals global regulation in response to CO2 supplementation in oleaginous microalga Coccomyxa subellipsoidea C-169. Biotechnol Biofuels 9:151. https://doi.org/10.1186/s13068-016-0571-5
Ruiz-Domínguez MC, Vaquero I, Obregón V, de laMorena B, Vílchez C, Vega JM (2015) Lipid accumulation and antioxidant activity in the eukaryotic acidophilic microalga Coccomyxa sp. (strain onubensis) under nutrient starvation. J Appl Phycol 27:1099–1108. https://doi.org/10.1007/s10811-014-0403-6
Tripathi S, Choudhary S, Poluri KM (2021) Insights into lipid accumulation features of Coccomyxa sp. IITRSTKM4 under nutrient limitation regimes. Environ Technol Innov 24:101786. https://doi.org/10.1016/j.eti.2021.101786
Verma V, Bhatti S, Huss VAR, Colman B (2009) Photosynthetic inorganic carbon acquisition in an acid-tolerant, free-living species of Coccomyxa (Chlorophyta). J Phycol 45:847–854. https://doi.org/10.1111/j.1529-8817.2009.00718.x
Wang C, Wang Z, Luo F, Li Y (2017) The augmented lipid productivity in an emerging oleaginous model alga Coccomyxa subellipsoidea by nitrogen manipulation strategy. World J Microbiol Biotechnol 33:160. https://doi.org/10.1007/s11274-017-2324-4
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We thank Suzanne Adam, PhD, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.
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This work was supported by the Strategic Research Foundation Grant-aided Project for Private Universities from Ministry of Education, Culture, Sport, Science, and Technology, Japan (S1411005); the Research Institute for Science and Technology of Kogakuin University for a special Grant-in-Aid to earn KAKENHI by the Japan Society for the Promotion of Science.
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NA, EK and KF conceived the study, EK and RM aided with study design and analysis. NA drafted the manuscript and all authors edited the manuscript. All authors have read and approved the final version.
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Aburai, N., Kitajima, E., Morita, R. et al. Nitrogen-assisted lipid production by biofilms of aerial microalga Coccomyxa subellipsoidea KGU-D001 in the aerial phase. Arch Microbiol 205, 60 (2023). https://doi.org/10.1007/s00203-022-03389-5
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DOI: https://doi.org/10.1007/s00203-022-03389-5