Abstract
The potential use of microalgae in advanced biological wastewater treatment processes has been actively studied due to their excellent nitrogen and phosphorus removal capabilities. This study investigated the inhibitory effects of free ammonia (FA) on microalgae under autotrophic, heterotrophic, and mixotrophic growth conditions, since the inhibitory effects in heterotrophic and mixotrophic modes has not been reported yet. Chlorella vulgaris were exposed to 3–20 mg-N L−1 of FA in the autotrophic, heterotrophic, and mixotrophic modes and the effects on growth, photosynthesis, and respiration were studied. The microalgal growth rate was 2–3 times greater in the mixotrophic mode than the other modes. Microalgal growth in the autotrophic mode was most vulnerable to FA and the growth inhibition was observed at FA concentration of ≥ 9 mg-N L−1. Similarly, the photosynthesis and respiration of C. vulgaris were inhibited at FA concentrations higher than 12 mg-N LT−1. The removal of carbon and ammonia was greater in the mixotrophic mode than the other modes. The ammonia removal by microalgae increased in proportion to the FA concentration unlike the carbon removal. This was attributed to the ammonium accumulation in microalgae due to the proton imbalance and differences in intracellular and external pH conditions, which were caused by the presence of excess FA in water. Overall, the results show that the mixotrophic microalgae have greater tolerance to FA, and hence, greater potential for use in treatment of wastewaters having high FA concentrations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ali W, Takaijudin H, Yusof KW, Osman M, Abdurrasheed AS (2021) The common approaches of nitrogen removal in bioretention system. Sustainability 13(5):2575, DOI: https://doi.org/10.3390/su13052575
Azov Y, Goldman JC (1982) Free ammonia inhibition of algal photosynthesis in intensive cultures. Applied and Environmental Microbiology 43(4):735–739, DOI: https://doi.org/10.1128/aem.43.4.735-739.1982
Cai T, Park SY, Li Y (2013) Nutrient recovery from wastewater streams by microalgae: Status and prospects. Renewable and Sustainable Energy Reviews 19:360–369, DOI: https://doi.org/10.1016/j.rser.2012.11.030
Cheirsilp B, Torpee S (2012) Enhanced growth and lipid production of microalgae under mixotrophic culture condition: Effect of light intensity, glucose concentration and fed-batch cultivation. Bioresource Technology 110:510–516, DOI: https://doi.org/10.1016/j.biortech.2012.01.125
Chojnacka K, Marquez-Rocha FJ (2004) Kinetic and stoichiometric relationships of the energy and carbon metabolism in the culture of microalgae. Biotechnology 3(1):21–34, DOI: https://doi.org/10.3923/biotech.2004.21.34
Chojnacka K, Noworyta A (2004) Evaluation of Spirulina sp. growth in photoautotrophic, heterotrophic and mixotrophic cultures. Enzyme and Microbial Technology 34(5):461–465, DOI: https://doi.org/10.1016/j.enzmictec2003.12.002
Diner BA (2001) Amino acid residues involved in the coordination and assembly of the manganese cluster of photosystem II. Proton-coupled electron transport of the redox-active tyrosines and its relationship to water oxidation. Biochimica et Biophysica Acta (BBA) — Bioenergetics 1503(1–2):147–163, DOI: https://doi.org/10.1016/S0005-2728(00)00220-6
Drath M, Kloft N, Batschauer A, Marin K, Novak J, Forchhammer K (2008) Ammonia triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiology 147(1):206–215, DOI: https://doi.org/10.1104/pp.108.117218
El-Mashad HM, Zeeman G Loon WKP, Bot GPA, Lettinga G (2004) Effect of temperature and temperature fluctuation on thermophilic anaerobic digestion of cattle manure. Bioresource Technology 95(2): 191–201, DOI: https://doi.org/10.1016/j.biortech.2003.07.013
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303(5665):1831–1838, DOI: https://doi.org/10.1126/science.1093087
Gutierrez J, Kwan TA, Zimmerman JB, Peccia J (2016) Ammonia inhibition in oleaginous microalgae. Algal Research 19:123–127, DOI: https://doi.org/10.1016/j.algal.2016.07.016
Hii YS, Soo CL, Chuah TS, Mohd-Azmi A, Abol-Munafi AB (2011) Interactive effect of ammonia and nitrate on the nitrogen uptake by Nannochloropsis sp. Journal of Sustainability and Management 6(1):60–68
Jiang R, Qin L, Feng S, Huang D, Wang Z, Zhu S (2021) The joint effect of ammonium and pH on the growth of Chlorella vulgaris and ammonium removal in artificial liquid digestate. Bioresource Technology 325:124690, DOI: https://doi.org/10.1016/j.biortech.2021.124690
Kadam PC, Boone DR (1996) Influence of pH on ammonia accumulation and toxicity in halophilic, methylotrophic methanogens. Applied Environmental Microbiology 62(12):4486–4492, DOI: https://doi.org/10.1128/AEM.62.12.4486-4492.1996
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. Microbial Cell Factories 17(1):36, DOI: https://doi.org/10.1186/s12934-018-0879-x
Korner S, Das SK, Veensta S, Vermaat JE (2001) The effect of pH variation at the ammonium/ammonia equilibrium in wastewater and its toxicity to Lemna gibba. Aquatic Botany 71(1): 71–78, DOI: https://doi.org/10.1016/S0304-3770(01)00158-9
Markou G, Depraetere O, Muylaert K (2016) Effect of ammonia on the photosynthetic activity of Arthrospira and Chlorella A study on chlorophyll fluorescence and electron transport. Algal Research 16:449–457, DOI: https://doi.org/10.1016/j.algal.2016.03.039
Mohammed-Nour A, Al-Sewailem M, El-Naggar AH (2019) The influence of alkalization and temperature on ammonia recovery from cow manure and the chemical properties of the effluents. Sustainability 11(8):2441, DOI: https://doi.org/10.3390/su11082441
Mohsenpour SF, Hennige S, Willoughby N, Adeloye A, Gurierrez T (2021) Integrating micro-algae into wastewater treatment: A review. Science of the Total Environment 752(15):142168, DOI: https://doi.org/10.1016/j.scitotenv.2020.142168
Nirmalakhandan N, Selvaratnam T, Henkanatte-Gedera SM, Tchinda D, Abeysiriwardana-Arachchige ISA, Delanka-Pedige HMK, Munasinghe-Arachchige SP, Zhang Y, Holguin FO, Lammers PJ (2019) Algal wastewater treatment: Photoautotrophic vs. mixotrophic processes. Algal Research 41:101569, DOI: https://doi.org/10.1016/j.algal.2019.101569
Perez-Garcia O, Escalante FM, De-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: Metabolism and potential products. Water Research 45(1):11–36, DOI: https://doi.org/10.1016/j.watres.2010.08.037
Qian W, Peng Y, Li X, Zhang Q, Ma B (2017) The inhibitory effects of free ammonia on ammonia oxidizing bacteria and nitrite oxidizing bacteria under anaerobic condition. Bioresource Technology 243:1247–1250, DOI: https://doi.org/10.1016/j.biortech.2017.07.119
Rajagopal R, Massé DI, Singh G (2013) A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresource Technology 143:632–641, DOI: https://doi.org/10.1016/j.biortech.2013.06.030
Silva FJR, Lima FRS, Vale DA, Carmo MV (2013) High levels of total ammonia nitrogen as NH4+ are stressful and harmful to the growth of Nile tilapia juveniles. Acta Scientiarum Biological Sciences 35(4):475–481
Tam NFY, Wong YS (1996) Effect of ammonia concentrations on growth of Chlorella vulgaris and nitrogen removal from media. Bioresource Technology 57:45–50, DOI: https://doi.org/10.1016/0960-8524(96)00045-4
Terrado R, Monier A, Edgar R, Lovejoy C (2015) Diversity of nitrogen assimilation pathways among microbial photosynthetic eukaryotes. Journal of Phycology 51(3):490–506, DOI: https://doi.org/10.1111/jpy.12292
Walters WW, Chai J, Hastings MG (2019) Theoretical phase resolved ammonia-ammonium nitrogen equilibrium isotope exchange fractionations: Applications for tracking atmospheric ammonia gas-to-particle conversion. ACS Earth and Space Chemistry 3(1):79–89, DOI: https://doi.org/10.1021/acsearthspacechem.8b00140
White DA, Pagarette A, Rooks P, Ali ST (2013) The effect of sodium bicarbonate supplementation on growth and biochemical composition of marine microalgae cultures. Journal of Applied Phycology 25:153–165, DOI: https://doi.org/10.1007/s10811-012-9849-6
Wollmann F, Dietze S, Ackermann J, Bley T, Walther T, Steingroewer J, Krujatz F (2019) Microalgae wastewater treatment: Biological and technological approaches. Engineering in Life Sciences 19(12):860–871, DOI: https://doi.org/10.1002/elsc.201900071
Wu C, Xiong W, Dai J, Wu Q (2016) Kinetic flux profiling dissects nitrogen utilization pathways in the oleaginous green alga Chlorella protothecoides. Journal of Phycology 52(1):116–124, DOI: https://doi.org/10.1111/jpy.12374
Yeh KL, Chang JS, Chen WM (2010) Effect of light supply and carbon source on cell growth and cellular composition of a newly isolated microalga Chlorella vulgaris ESP-31. Engineering in Life Sciences 10(3):201–208, DOI: https://doi.org/10.1002/elsc.200900116
Zhan J, Rong J, Wang Q (2017) Mixotrophic cultivation, a preferable microalgae cultivation mode for biomass/bioenergy production, and bioremediation, advances and prospect. International Journal of Hydrogen Energy 42(12):8505–8517, DOI: https://doi.org/10.1016/j.ijhydene.2016.12.021
Zheng C, Zhao L, Zhou X, Fu Z, Li A (2013) Treatment technologies for organic wastewater. Environmental Science 249–286, DOI: https://doi.org/10.5772/52665
Acknowledgments
This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP) (Grant number 2019R1A2C1084155).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kim, EJ., Jho, E.H., Jang, HS. et al. Inhibition Effects of Free Ammonia (FA) on the Rates of Growth, Photosynthesis and Respiration of Chlorella vulgaris. KSCE J Civ Eng 26, 2567–2574 (2022). https://doi.org/10.1007/s12205-022-1430-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12205-022-1430-5