Abstract
Microalgal density is one of the factors affecting bioremediation efficiency, but literature on the density that efficiently removes nitrogen and phosphorus from aquaculture wastewater is still very limited. Thus, this study was conducted to optimize the density of Isochrysis galbana, Nannochlorum sp., and Tetraselmis tetrahele to efficiently remove inorganic N (NH3-N, NO2-N) and P. Three densities such as low, medium, and high with an optical density at 680 nm of 0.1, 0.2, and 0.3, respectively, were evaluated for 12 days. Results showed that medium density was good for Isochrysis galbana and Nannochlorum sp. in the removal of both N and P with rates reaching 97.93% and 84.07%, 94.25% and 93.39%, and 59.39% and 71.65% for NH3-N, NO2-N, and P, respectively. For Tetraselmis tetrahele, the low density efficiently removed N, while the high density effectively removed P with the highest removal of 99.16%, 97.5%, and 51.55% for NH3-N, NO2-N, and P, respectively. Specific growth rates of Isochrysis galbana and Tetraselmis tetrahele were affected by density; the lower the densities, the higher their growth rates. The three densities did not differ significantly in Nannochlorum sp. Isochrysis galbana and Nannochlorum sp. biomass productivity were high in medium and high densities, while low and medium densities for Tetraselmis tetrahele. Overall, the optimization of microalgal density is beneficial in the efficient removal of nitrogen and phosphorus from aquaculture wastewater.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Data availability
The data used to support the findings of this study are available from the corresponding author upon request.
Code availability
Not available.
References
Abdelfattah A, Ali SS, Ramadan H, El-Aswar EL, Eltawab R, Ho S, Elsamahy T, Li S, El-Sheekh MM, Schagerl M, Kornaros M, Sun J (2023) Microalgae-based wastewater treatment: mechanisms, challenges, recent advances, and future prospects. Environ Sci Ecotechnol 13:100205. https://doi.org/10.1016/j.ese.2022.100205
Abdel-Raouf N, Al-Homaidan AA, Ibraheem IBM (2012) Microalgae and wastewater treatment. Saude J Biol Sci 9:257–275. https://doi.org/10.1016/j.sjbs.2012.04.005
Abreu MH, Pereira R, Yarish C, Buschmann AH, Sousa-Pinto I (2011) IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 312:77–87. https://doi.org/10.1016/j.aquaculture.2010.12.036
Ahmed A, Jyothi N, Rames A (2017) Improved ammonium removal from industrial wastewater through systematic adaptation of wild type Chlorella pyrenoidosa. Water Sci Technol 75(1):182–188. https://doi.org/10.2166/wst.2016.507
Alam MA, Wan C, Zhao XQ, Chen LJ, Chang JS, Bai FW (2015) Enhanced removal of Zn2+ or Cd2+ by the flocculating Chlorella vulgaris JSC-7. J Hazard Mater 289:38–45. https://doi.org/10.1016/j.jhazmat.2015.02.012
Amaro HM, Salgado EM, Nunes OC, Pires JC, Esteves AF (2023) Microalgae systems - environmental agents for wastewater treatment and further potential biomass valorization. J Environ Manage 337:117678. https://doi.org/10.1016/j.jenvman.2023.117678
Aníbal J, Madeira HT, Carvalho LF, Esteves E, Veiga-Pires C, Rocha C (2013) Macroalgae mitigation potential for fish aquaculture effluents: an approach coupling nitrogen uptake and metabolic pathways using Ulva rigida and Enteromorpha clathrata. Environ Sci Pollut Res 21:13324–13334. https://doi.org/10.1007/s11356-013-2427-x
Ansari FA, Singh P, Guldhe A, Bux F (2017) Microalgal cultivation using aquaculture wastewater: integrated biomass generation and nutrient remediation. Algal Res 21:169–177. https://doi.org/10.1016/j.algal.2016.11.015
Barsanti L, Gualtieri P (2006) Algae: anatomy, biochemistry, and biotechnology. CRC Press, Boca Raton
Biji X, Sekar M, Vamsi B (2016) Microalgae culture media and glass ware. In: Xavier B, Ranjan R, Megarajan S, Ghosh S, Edward LL, Dash B (eds). Training manual on live feed for marine finfish and shellfish culture. CMFRI Training manual Ser. No 9, pp 15-25. https://www.researchgate.net/publication/304990172_Live_feed_for_marine_finfish_and_shellfish_culture. Accessed 28 Oct 2022
Cai T, Park SY, Li Y (2013) Nutrient recovery from wastewater streams by microalgae: status and prospects. Renew Sustain Energy Rev 19:360–369. https://doi.org/10.1016/j.rser.2012.11.030
Chalivendra S (2014) Bioremediation of wastewater using microalgae. Dissertation. University of Dayton, Dayton, Ohio. http://rave.ohiolink.edu/etdc/view?acc_num=dayton1418994496
Cheban L, Malischuk I, Marchenko M (2015) Cultivating desmodesmus armatus (chod.) Hegew. in recirculating aquaculture systems (RAS) wastewater. Fish Aquat Life 23(3):155–162. https://doi.org/10.1515/aopf-2015-0018
Choi HJ, Lee SM (2012) Effects of microalgae on the removal of nutrients from wastewater: various concentrations of Chlorella vulgaris. Environ Eng Res 17(S1):S3–S8. https://doi.org/10.4491/eer.2012.17.S1.S3
Cohen RA, Fong P (2005) Experimental evidence supports the use of δ15N content of the opportunistic green macroalga Enteromorpha intestinalis (Chlorophyta) to determine nitrogen sources to estuaries. J Phycol 41:287–293. https://doi.org/10.1111/j.1529-88172005.04022x
Collos Y, Harrison PJ (2014) Acclimation and toxicity of high ammonium concentrations to unicellular algae. Mar Pollut Bull 80:8–23. https://doi.org/10.1016/j.marpolbul.2014.01.006
Du R, Liu L, Wang A, Wang Y (2013) Effects of temperature, algae biomass, and ambient nutrient on the absorption of dissolved nitrogen and phosphate by rhodophyte Gracilaria asiatica. Chin J Oceanol Limnol 31(2):353–365. https://doi.org/10.1007/s00343-013-2114-2
Food and Agriculture Organization (FAO) of the United Nations (2014) The state of world fisheries and aquaculture, opportunities and challenges 2020. http://www.fao.org/3/a-i3720e.pdf. Accessed 22 Dec 2022
Food and Agriculture Organization (FAO) of the United Nations (2020) The state of world fisheries and aquaculture 2020. https://www.fao.org/state-of-fisheries-aquaculture. Accessed 28 Dec 2022
Ferrer-Alvarez YI, Ortega-Clemente LA, Pérez-Legaspi IA, Hernández-Vergara MP, Robledo-Narvaez PN (2015) Growth of Chlorella vulgaris and Nannochloris oculata in effluents of tilapia farming for the production of fatty acids with potential in biofuels. African Journal of Biotechnology, 14(20):1710–1717. https://doi.org/10.5897/AJB2015.14421
Ferriols VMEN, Saclauso CA, Fortes NR, Toledo NA, Pahila IG (2013) Effect of elevated carbon dioxide and phosphorus levels on nitrogen uptake, lipid content and growth of Tetraselmis sp. J Fish Aquat Sci 8:659–672. https://doi.org/10.3923/jfas.2013.659.672
Gani P, Sunar NM, Matias-Peralta H, Abdul Latiff AA, Abdul Razak AR (2016) Influence of initial cell concentrations on the growth rate and biomass productivity of microalgae in domestic wastewater. Appl Ecol Environ Res 14(2):399–409. https://doi.org/10.15666/aeer/1402_399409
Goh PS, Lau WJ, Ismail AF, Samawati Z, Liang YY, Kanakaraju D (2023) Microalgae-enabled wastewater treatment: a sustainable strategy for bioremediation of pesticides. Water 15(1):70. https://doi.org/10.3390/w15010070
Guo Z, Liu Y, Guo H, Yan S, Mu J (2013) Microalgae cultivation using an aquaculture wastewater as growth medium for biomass and biofuel production. J Environ Sci Suppl 1:S85–S88. https://doi.org/10.1016/S1001-0742(14)60632-X
Hempel N, Petrick I, Behrendt F (2012) Biomass productivity and productivity of fatty acids and amino acids of microalgae strains as key characteristics of suitability for biodiesel production. J Appl Phycol 24:1407–1418. https://doi.org/10.1007/s10811-012-9795-3
Hu W (2014) Dry weight and cell density of individual algal and cyanobacterial cells for algae research and development. Master of Science Thesis. University of Missouri-Columbia. https://hdl.handle.net/10355/46477
Jia H, Yuan Q (2018) Ammonium removal using algae bacteria consortia: the effect of ammonium concentration, algae biomass, and light. Biodegradation 29(2):105–115. https://doi.org/10.1007/s10532-017-9816-7
Kawaroe M, Hwangbo J, Augustine D, Putr HA (2015) Comparison of density, specific growth rate, biomass weight, and doubling time of microalgae Nannochloropsis sp. cultivated in open raceway pond and photobioreactor. AACL BIOFLUX Aquac Aquar Conserv Legis Int J Bioflux Soc 8(15):740–750
Kumar KP, Krishna SV, Naidua SS, Verma K, Bhagawan D, Himabindu V (2019) Biomass production from microalgae Chlorella grown in sewage, kitchen wastewater using industrial CO2 emissions: comparative study. Carbon Resour Convers 2:126–133. https://doi.org/10.1016/j.crcon.2019.06.002
Kurosu O (2001) Nitrogen removal from wastewater in microalgal-bacterial treatment ponds. https://nature.berkeley.edu/classes/es196/projects/2001final/Kurosu.pdf. Accessed 29 November 2022
Lage S, Toffolo A, Gentili FG (2021) Microalgal growth, nitrogen uptake and storage, and dissolved oxygen production in a polyculture based-open pond fed with municipal wastewater in northern Sweden. Chemosphere 276. https://doi.org/10.1016/j.chemosphere.2021.130122
Lananan F, Abdul Hamid SH, Sakinah Din WN, Ali N, Khatoon H, Jusoh A, Endut A (2014) Symbiotic bioremediation of aquaculture wastewater in reducing ammonia and phosphorus utilizing effective microorganism (EM-1) and microalgae (Chlorella sp.). Int Biodeterior Biodegradation 95:127–134. https://doi.org/10.1016/j.ibiod.2014.06.013
Larsdotter K, la Cour Jansen J, Dalhammar G (2010) Phosphorus removal from wastewater by microalgae in Sweden - a year-round perspective. Environmental Technology 31(2):117-123. https://doi.org/10.1080/09593330903382815
Lau PS, Tam NFY, Wong YS (1995) Effect of algal density on nutrient removal from primary settled wastewater. Environ Pollut 89(1):59–66. https://doi.org/10.1016/0269-7491(94)00044-E
Li S, Mubashar M, Qin Y, Nie X, Zhang X (2022) Aquaculture waste nutrient removal using microalgae with floating permeable nutrient uptake system (FPNUS). Biores Technol 347:126338. https://doi.org/10.1016/j.biortech.2021.12633
Liang Z, Liu Y, Ge F, Xu Y, Tao N, Peng F, Wong M (2013) Efficiency assessment and pH effect in removing nitrogen and phosphorus by algae-bacteria combined system of Chlorella vulgaris and Bacillus licheniformis. Chemosphere 92(10):1383–1389. https://doi.org/10.1016/j.chemosphere.2013.05.014
Lugo L, Thorarinsdottir RI, Bjornsson S, Palsson O, Skulason H, Johannsson S, Brynjolfsson S (2020) Remediation of aquaculture wastewater using the microalga Chlorella sorokiniana. Water 12(11):3144. https://doi.org/10.3390/w12113144
Macchiavello J, Bulboa C (2014) Nutrient uptake efficiency of Gracilaria chilensis and Ulva lactuca in an IMTA system with the red abalone Haliotis rufescens. Lat Am J Aquat Res 45:523–533. https://doi.org/10.3856/vol42-issue3-fulltext-12
Martinez MR, Chakroff CL, Pantastico JF (1975) Direct counting techniques using the haemacymeter. Phil Agri 55:43–50
Piñosa LAG (2018) Influence of colonization time on phytoperiphyton growth during wet and dry seasons in brackish water pond. J Appl Phycol 30:3633–3641. https://doi.org/10.1007/s10811-018-1497-z
Prabu E, Santhiya AAV (2016) An overview of bioremediation towards aquaculture. J Aqua Trop 31(3–4):155–164
Saccardo A, Bezzo F, Sforza E (2022) Microalgae growth in ultra-thin steady-state continuous photobioreactors: assessing self-shading effects. Front Bioeng Biotechnol 10. https://doi.org/10.3389/fbioe.2022.977429
Samori G, Samori C, Guerrini F, Pistocchi R (2013) Growth and nitrogen removal capacity of Desmodesmus communis and of a natural microalgae consortium in a batch culture system in view of urban wastewater treatment: part I. Water Res 47(2):791–801. https://doi.org/10.1016/j.watres.2012.11.006
Sedlak R (1991) Phosphorus and nitrogen removal from municipal wastewater: principles and practice, 2nd edn. Lewis Publisher, New York
Sirirustananun N (2016) The suitable stocking density to growth of macroalgae Spirogyra spp. and its ability of ammonia nitrogen removal. Int J Agric Technol 12(3):533–543
Skriptsova AV, Miroshnikova NV (2011) Laboratory experiment to determine the potential of two macroalgae from the Russian Far-East as biofilters for integrated multi-trophic aquaculture (IMTA). Bioresour Technol 102:3149–3154. https://doi.org/10.1016/j.biortech.2010.10.093
Sousa C, Sousa H, Vale F, SimÕes M (2021) Microalgae-based bioremediation of wastewaters - influencing parameters and mathematical growth modelling. Chem Eng J 425:131412. https://doi.org/10.1016/j.cej.2021.131412
Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis, 2nd end. Fisheries Research Board of Canada
Su Y, Mennerich A, Urban B (2012) Comparison of nutrient removal capacity and biomass settleability of four high-potential microalgal species. Biores Technol 124:157–162
Talbot P, de la Noue J (1993) Tertiary treatment of wastewater with Phormidium bohneri (Schmidle) under various light and temperature conditions. Water Res 27(1):153–159. https://doi.org/10.1016/0043-1354(93)90206-W
Teichberg M, Heffner LR, Fox S, Valiela I (2007) Nitrate reductase and glutamine synthetase activity, internal N pools, and growth of Ulva lactuca: responses to long and short-term N supply. Mar Biol 151:1249–1259. https://doi.org/10.1007/s00227-006-0561-4
Torres EM, Hess D, McNeil BT, Guy T, Quinn JC (2017) Impact of inorganic contaminants on microalgae productivity and bioremediation potential. Ecotoxicol Environ Saf 139:367–376. https://doi.org/10.1016/j.ecoenv.2017.01.034
Tossavainen M, Lahti K, Edelmann M, Eskola R, Lampi AM, Piironen V, Korvonen P, Ojala A, Romantschuk M (2018) Integrated utilization of microalgae cultured in aquaculture wastewater: wastewater treatment and production of valuable fatty acids and tocopherols. J Appl Phycol 31:1753–1763. https://doi.org/10.1007/s10811-018-1689-6
Viegas C, Gouveia L, Goncalves M (2021) Aquaculture wastewater treatment through microalgal. Biomass potential applications on animal feed, agriculture, and energy. J Environ Manag 286:112187. https://doi.org/10.1016/j.jenvman.2021.112187
Walker PJ, Mohan CV (2009) Viral disease emergence in shrimp aquaculture: origins, impact and the effectiveness of health management strategies. Rev Aquac 1(2):125–154. https://doi.org/10.1111/j.1753-5131.2009.01007.x
Zhang L, Han J, Ma S, Zhang Y, Wang Y, Xu J (2023) Comprehensive evaluation of growth characteristics, nitrogen removal capacity, and nutritional properties of three diet microalgae. Front Mar Sci 10. https://doi.org/10.3389/fmars.2023.1117043
Acknowledgements
The authors wish to acknowledge the University of the Philippines Visayas In-house Research Grant for the financial support. Special thanks to Dr. Liah C. Catedrilla for reading the manuscript, Professor Roman C. Sanares for the statistical advice, and the Institute of Aquaculture of the University of the Philippines Visayas, College of Fisheries and Ocean Sciences, for the assistance and support.
Funding
The study was funded by the University of the Philippines Visayas In-house Research Grant under the Office of the Vice Chancellor for Research and Extension.
Author information
Authors and Affiliations
Contributions
Both authors had significant contributions to the conduct of the experiment and in the preparation of the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Handling Editor: Ronan Sulpice
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
Piñosa, L.A.G., Apines-Amar, M.J.S. Optimization of stocking density for Isochrysis galbana, Nannochlorum sp., and Tetraselmis tetrahele in the bioremediation of aquaculture wastewater. Aquacult Int 32, 3597–3616 (2024). https://doi.org/10.1007/s10499-023-01340-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-023-01340-z