Abstract
Coupling algal cultivation with wastewater treatment due to their potentials to alleviate energy crisis and reduce environmental burden has attracted the increased attention in recent years. However, these microalgal-based processes are challenging since daily and seasonal temperature fluctuation may affect microalgal growth in wastewater, and the effects of the temperature regimes on microalgal biomass production and wastewater nutrient removal remain unclear. In this study, Chlorella vulgaris was continuously cultured for 15 days in municipal wastewater to investigate the effects on the algal biomass and wastewater nutrient removal in three temperature regimes: (1) low temperature (4 °C), (2) high temperature (35 °C), and (3) alternating high-low temperature (35 °C in the day: 4 °C at night). Compared with the other two temperature regimes, the high-low temperature conditions generated the most biomass (1.62 g L-1), the highest biomass production rate (99.21 mg L-1 day-1), and most efficient removal of COD, TN, NH3-N, and TP (83.0%, 96.5%, 97.8%, and 99.2%, respectively). In addition, the polysaccharides, proteins, lipid content, and fatty acid methyl ester composition analysis indicates that in alternating high-low temperature condition, biomass production increased the potential for biofuel production, and there was the highest lipid content (26.4% of total dry biomass). The results showed that the nutrients except COD were all efficiently removed in these temperature conditions, and the alternating high-low temperature condition showed great potential to generate algal biomass and alleviate the wastewater nutrients. This study provides some valuable information for large-scale algal cultivation in wastewater and microalgal-based wastewater treatments.
Similar content being viewed by others
References
Aussant J, Guiheneuf F, Stengel DB (2018) Impact of temperature on fatty acid composition and nutritional value in eight species of microalgae. Appl Microbiol Biotechnol 102(12):5279–5297. https://doi.org/10.1007/s00253-018-9001-x
Aboushanab RAI, Ji MK, Kim HC, Paeng KJ, Jeon BH (2013) Microalgal species growing on piggery wastewater as a valuable candidate for nutrient removal and biodiesel production. J Environ Manag 115(3):257–264. https://doi.org/10.1016/j.jenvman.2012.11.022
Ball SG, Dirick L, Decq A, Martiat JC, Matagne R (1990) Physiology of starch storage in the monocellular alga Chlamydomonas reinhardtii. Plant Sci 66(1):1–9. https://doi.org/10.1016/0168-9452(90)90162-H
Banerjee A, Sharma R, Chisti Y, Banerjee UC (2002) Botryococcus braunii: a renewable source of hydrocarbons and other chemicals. Crit Rev Biotechnol 22(3):245–279. https://doi.org/10.1080/07388550290789513
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Biochem Cell Biol 37(8):911–917. https://doi.org/10.1139/o59-099
Butterwick C, Heaney SI, Talling J (2004) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw Biol 50(2):291–300. https://doi.org/10.1111/j.1365-2427.2004.01317.x
Carvalho AP, Silva SO, Baptista JM, Malcata FX (2011) Light requirements in microalgal photobioreactors: an overview of biophotonic aspects. Appl Microbiol Biotechnol 89(5):1275–1288. https://doi.org/10.1007/s00253-010-3047-8
Feng Y, Li C, Zhang D (2011) Lipid production of Chlorella vulgaris cultured in artificial wastewater medium. Bioresour Technol 102(1):101–105. https://doi.org/10.1016/j.biortech.2010.06.016
Ferro L, Gorzsás A, Gentili FG, Funk C (2018) Subarctic microalgal strains treat wastewater and produce biomass at low temperature and short photoperiod. Algal Res 35:160–167. https://doi.org/10.1016/j.algal.2018.08.031
Foladori P, Petrini S, Andreottola G (2018) Evolution of real municipal wastewater treatment in photobioreactors and microalgae-bacteria consortia using real-time parameters. Chem Eng J 345:507–516. https://doi.org/10.1016/j.cej.2018.03.178
Gao F, Peng YY, Li C, Yang GJ, Deng YB, Xue B, Guo YM (2018) Simultaneous nutrient removal and biomass/lipid production by Chlorella sp. in seafood processing wastewater. Sci Total Environ 640-641:943–953. https://doi.org/10.1016/j.scitotenv.2018.05.380
Georgianna DR, Mayfield SP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488(7411):329–335. https://doi.org/10.1038/nature11479
González-Fernández C, Mahdy A, Ballesteros I, Ballesteros M (2016) Impact of temperature and photoperiod on anaerobic biodegradability of microalgae grown in urban wastewater. Int Biodeterior Biodegradation 106:16–23. https://doi.org/10.1016/j.ibiod.2015.09.016
Gómez-Serrano C, Morales-Amaral MM, Acién FG, Escudero R, Fernández-Sevilla JM, Molina-Grima E (2015) Utilization of secondary-treated wastewater for the production of freshwater microalgae. Appl Microbiol Biotechnol 99(16):6931–6944. https://doi.org/10.1007/s00253-015-6694-y
Ho SH, Chen CY, Chang JS (2012) Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113:244–252. https://doi.org/10.1016/j.biortech.2011.11.133
Huo S, Wang Z, Zhu S, Zhou W, Dong R, Yuan Z (2012) Cultivation of Chlorella zofingiensis in bench-scale outdoor ponds by regulation of pH using dairy wastewater in winter, South China. Bioresour Technol 121:76–82. https://doi.org/10.1016/j.biortech.2012.07.012
Ji MK, Kim H, Sapireddy VR, Yun HS, Aboushanab RAI, Choi JY, Lee W, Timmes TC, Inamuddin JB (2013) Simultaneous nutrient removal and lipid production from pretreated piggery wastewater by Chlorella vulgaris YSW-04. Appl Microbiol Biotechnol 97(6):2701–2710. https://doi.org/10.1007/s00253-012-4097-x
Khiewwijit R, Rijnaarts H, Temmink H, Keesman KJ (2018) Glocal assessment of integrated wastewater treatment and recovery concepts using partial nitritation/anammox and microalgae for environmental impacts. Sci Total Environ 628-629:74–84. https://doi.org/10.1016/j.scitotenv.2018.01.334
Laurens LML, Dempster TA, Jones HDT, Wolfrum EJ, Van Wychen S, Mcallister JSP, Rencenberger M, Parchert KJ, Gloe LM (2012) Algal biomass constituent analysis: method uncertainties and investigation of the underlying measuring chemistries. Anal Chem 84(4):1879–1887. https://doi.org/10.1021/ac202668c
Lee CS, Oh H, Oh H, Kim H, Ahn C (2016) Two-phase photoperiodic cultivation of algal-bacterial consortia for high biomass production and efficient nutrient removal from municipal wastewater. Bioresour Technol 200:867–875. https://doi.org/10.1016/j.biortech.2015.11.007
Li Y, Chen YF, Chen P, Min M, Zhou W, Martinez B, Zhu J, Ruan R (2011) Characterization of a microalga Chlorella sp. adapted to highly concentrated municipal wastewater for nutrient removal and biodiesel production. Bioresour Technol 102:5138–5144. https://doi.org/10.1016/j.biortech.2011.01.091
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275. https://doi.org/10.1515/bchm2.1951.286.1-6.270
Luo L, He H, Yang C, Wen S, Zeng G, Wu M, Zhou Z, Lou W (2016) Nutrient removal and lipid production by Coelastrella sp. in anaerobically and aerobically treated swine wastewater. Bioresour Technol 216:135–141. https://doi.org/10.1016/j.biortech.2016.05.059
Lu Q, Han P, Chen F, Liu T, Leng L, Li J, Zhou W (2019) A novel approach of using zeolite for ammonium toxicity mitigation and value-added Spirulina cultivation in wastewater. Bioresour Technol 280:127–135. https://doi.org/10.1016/j.biortech.2019.02.042
Ma C, Wen H, Xing D, Pei X, Zhu J, Ren N, Liu B (2017) Molasses wastewater treatment and lipid production at low temperature conditions by a microalgal mutant Scenedesmus sp. Z-4. Biotechnol Biofuels 10(1):111. https://doi.org/10.1186/s13068-017-0797-x
Ma X, Zhou W, Fu Z, Cheng Y, Min M, Liu Y, Zhang Y, Chen P, Ruan R (2014) Effect of wastewater-borne bacteria on algal growth and nutrients removal in wastewater-based algae cultivation system. Bioresour Technol 167:8–13. https://doi.org/10.1016/j.biortech.2014.05.087
Mennaa FZ, Arbib Z, Perales JA (2015) Urban wastewater treatment by seven species of microalgae and an algal bloom: Biomass production, N and P removal kinetics and harvestability. Water Res 83:42–51. https://doi.org/10.1016/j.renene.2016.01.090
Otondo A, Kokabian B, Stuartdahl S, Gude VG (2018) Energetic evaluation of wastewater treatment using microalgae, Chlorella vulgaris. J Environ Chem Eng 6(2):3213–3222. https://doi.org/10.1016/j.jece.2018.04.064
Přibyl P, Cepak V, Zachleder V (2012) Production of lipids in 10 strains of Chlorella and Parachlorella, and enhanced lipid productivity in Chlorella vulgaris. Appl Microbiol Biotechnol 94(2):549–561. https://doi.org/10.1007/s00253-012-3915-5
Ras M, Steyer JP, Bernard O (2013) Temperature effect on microalgae: a crucial factor for outdoor production. Rev Environ Sci Biotechnol 12(2):153–164. https://doi.org/10.1007/s11157-013-9310-6
Reitan KI, Rainuzzo JR, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30(6):972–979. https://doi.org/10.1111/j.0022-3646.1994.00972.x
Renaud SM, Thinh L, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211(1):195–214. https://doi.org/10.1016/S0044-8486(01)00875-4
Rice EW, Baird RB, Eaton AD, Clesceri LS (2012) Standard methods for the examination of water and wastewater, 22edn edn. American Public Health Association, American Water Works Association & Water Environment Federation, Washington
Shin HS, Hong SJ, Yoo C, Han MA, Lee H, Choi HK, Cho S, Lee CG, Cho BK (2016) Genome-wide transcriptome analysis revealed organelle specific responses to temperature variations in algae. Sci Rep 6(1):37770. https://doi.org/10.1038/srep37770
Smetana S, Sandmann M, Rohn S, Pleissner D, Heinz V (2017) Autotrophic and heterotrophic microalgae and cyanobacteria cultivation for food and feed: life cycle assessment. Bioresour Technol 245:162–170. https://doi.org/10.1016/j.biortech.2017.08.113
Sturm BSM, Lamer SL (2011) An energy evaluation of coupling nutrient removal from wastewater with algal biomass production. Appl Energy 88(10):3499–3506. https://doi.org/10.1016/j.apenergy.2010.12.056
Subhadra B (2011) Water management policies for the algal biofuel sector in the Southwestern United States. Appl Energy 88(10):3492–3498. https://doi.org/10.1016/j.apenergy.2010.10.024
Su ZF, Li X, Hu HY, Wu YH, Noguchi T (2011) Culture of Scenedesmus sp. LX1 in the modified effluent of a wastewater treatment plant of an electric factory by photo-membrane bioreactor. Bioresour Technol 102(17):7627–7632. https://doi.org/10.1016/j.biortech.2011.05.009
Wang H, Xiong H, Hui Z, Zeng X (2012) Mixotrophic cultivation of Chlorella pyrenoidosa with diluted primary piggery wastewater to produce lipids. Bioresour Technol 104:215–220. https://doi.org/10.1016/j.biortech.2011.11.020
Wang JH, Zhang TY, Dao GH, Xu XQ, Wang XX, Hu HY (2017) Microalgae-based advanced municipal wastewater treatment for reuse in waster bodies. Appl Microbiol Biotechnol 101(7):2659–2675. https://doi.org/10.1007/s00253-017-8184-x
Wang L, Min M, Li Y, Chen P, Chen Y, Liu Y, Wang Y, Ruan R (2010) Cultivation of green algae Chlorella sp. in different wastewaters from municipal wastewater treatment plant. Appl Biochem Biotechnol 162(4):1174–1186. https://doi.org/10.1007/s12010-009-8866-7
Wang Y, Guo W, Yen HW, Ho SH, Lo YC, Cheng CL, Ren N, Chang JS (2015) Cultivation of Chlorella vulgaris JSC-6 with swine wastewater for simultaneous nutrient/COD removal and carbohydrate production. Bioresour Technol 198(198):619–625. https://doi.org/10.1016/j.biortech.2015.09.067
Wang Y, Ho SH, Cheng CL, Guo WQ, Nagarajan D, Ren NQ, Lee D, Chang JS (2016) Perspectives on the feasibility of using microalgae for industrial wastewater treatment. Bioresour Technol 222:485–497. https://doi.org/10.1016/j.biortech.2016.09.106
Xu K, Zou X, Wen H, Xue Y, Zhao S, Li Y (2018) Buoy-bead flotation harvesting of the microalgae Chlorella vulgaris using surface-layered polymeric microspheres: a novel approach. Bioresour Technol 267:341–346. https://doi.org/10.1016/j.biortech.2018.07.065
Yan C, Muñoz R, Zhu L, Wang Y (2016a) The effects of various LED (light emitting diode) lighting strategies on simultaneous biogas upgrading and biogas slurry nutrient reduction by using of microalgae Chlorella sp. Energy 106:554–561. https://doi.org/10.1016/j.energy.2016.03.033
Yan C, Zhu L, Wang Y (2016b) Photosynthetic CO2 uptake by microalgae for biogas upgrading and simultaneously biogas slurry decontamination by using of microalgae photobioreactor under various light wavelengths, light intensities, and photoperiods. Appl Energy 178:9–18. https://doi.org/10.1016/j.apenergy.2016.06.012
Zhou D, Niu S, Xiong Y, Yang Y, Dong S (2014) Microbial selection pressure is not a prerequisite for granulation: dynamic granulation and microbial community study in a complete mixing bioreactor. Bioresour Technol 161:102–108. https://doi.org/10.1016/j.biortech.2014.03.001
Zhou W, Li Y, Min M, Hu B, Chen P, Ruan R (2011) Local bioprospecting for high-lipid producing microalgal strains to be grown on concentrated municipal wastewater for biofuel production. Bioresour Technol 102(13):6909–6919. https://doi.org/10.1016/j.biortech.2011.04.038
Zhu L, Wang Z, Shu Q, Takala J, Hiltunen E, Feng P, Yuan Z (2013) Nutrient removal and biodiesel production by integration of freshwater algae cultivation with piggery wastewater treatment. Water Res 47(13):4294–4302. https://doi.org/10.1016/j.watres.2013.05.004
Znad H, Ketife AMDA, Judd S, Almomani F, Vuthaluru HB (2018) Biroremediation and nutrient removal from wastewater by Chlorella vulgaris. Ecol Eng 110:1–7. https://doi.org/10.1016/j.ecoleng.2017.10.008
Zou X, Li Y, Xu K, Wen H, Shen Z, Ren X (2018) Microalgae harvesting by buoy-bead flotation process using bioflocculant as alternative to chemical flocculant. Algal Res 32:233–240. https://doi.org/10.1016/j.algal.2018.04.010
Funding
The authors would like to thank the National Natural Science Foundation of China (51478045), Key Laboratory of Degraded and Unused Land Consolidation Engineering of the Ministry of Land and Resources of China (SXDJ2017-6), supported by the Fund Project of Shaanxi Key Laboratory of Land Consolidation (2018-ZD04), and the Special Fund for Basic Scientific Research of Central Colleges, Chang’an University (300102299703 and 300102299708) for funding this project.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights and informed consent
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Xu, K., Zou, X., Wen, H. et al. Effects of multi-temperature regimes on cultivation of microalgae in municipal wastewater to simultaneously remove nutrients and produce biomass . Appl Microbiol Biotechnol 103, 8255–8265 (2019). https://doi.org/10.1007/s00253-019-10051-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-019-10051-6