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Treatment of Synthetic Ammonium Sulfate Wastewater by Mixed Culture of Chlorella pyrenoidosa and Enriched Nitrobacteria

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Abstract

Ammonium sulfate wastewater can cause eutrophication and black odor of water body. Although ammonia nitrogen can be used as nutrient of microalgae, high ammonia nitrogen levels could inhibit the growth of microalgae. Nitrobacteria can transform ammonia nitrogen into nitrate nitrogen. In this study, mono Chlorella pyrenoidosa culture (mono-C.py), synchronous mixed culture (mixed-a), and asynchronous mixed culture (mixed-b) systems were examined for their ability to treat ammonium sulfate wastewater. Nitrogen removal rate of mixed-b at the end of culture (52.96%) was higher than that of the mono-C.py (46.37%) and the mixed-a (39.11%). Higher total suspended solid concentration (2.40 g/L), crude protein yield (0.76 g/L), and heating value yield (35.73 kJ/L) were obtained in mixed-b, meanwhile with excellent settlement performance (91.43 ± 0.51%). Mechanism analysis of settlement showed that the relative abundance of floc-forming-related bacteria Sphingopyxis and Acidovorax were increased generally, while nitrification/denitrifying members were decreased in mixed-b along with the culture proceeding.

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All data generated or analyzed during this study are included in this published article.

References

  1. Luo X, Yan Q, Wang C, Luo C, Zhou N, Jian C (2015) Treatment of ammonia nitrogen wastewater in low concentration by two-stage ozonization. Int J Environ Res Public Health 12(9):11975–11987. https://doi.org/10.3390/ijerph120911975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Zhu G, Peng Y, Li B, Guo J, Yang Q, Wang S (2008) Biological removal of nitrogen from wastewater. Rev Environ Contam Toxicol 192:159–195. https://doi.org/10.1007/978-0-387-71724-1_5

    Article  CAS  PubMed  Google Scholar 

  3. Vergara C, Muñoz R, Campos JL, Seeger M, Jeison D (2016) Influence of light intensity on bacterial nitrifying activity in algal-bacterial photobioreactors and its implications for microalgae-based wastewater treatment. Int Biodeterior Biodegrad 114:116–121

    Article  CAS  Google Scholar 

  4. Li K, Liu Q, Fang F, Luo R, Lu Q, Zhou W, Huo S, Cheng P, Liu J, Addy M, Chen P, Chen D, Ruan R (2019) Microalgae-based wastewater treatment for nutrients recovery: a review. Bioresour Technol. https://doi.org/10.1016/j.biortech.2019.121934

    Article  PubMed  Google Scholar 

  5. Qin L, Liu L, Wang Z, Chen W, Wei D (2019) The mixed culture of microalgae Chlorella pyrenoidosa and yeast Yarrowia lipolytica for microbial biomass production. Bioprocess Biosyst Eng 42(9):1409–1419. https://doi.org/10.1007/s00449-019-02138-1

    Article  CAS  PubMed  Google Scholar 

  6. Xia A, Murphy JD (2016) Microalgal cultivation in treating liquid digestate from biogas systems. Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2015.12.010

    Article  PubMed  Google Scholar 

  7. Amenorfenyo DK, Huang XH, Zhang YL, Zeng QT, Zhang N, Ren JJ, Huang Q (2019) Microalgae brewery wastewater treatment: potentials, benefits and the challenges. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph16111910

    Article  PubMed  PubMed Central  Google Scholar 

  8. Han JC, Thomsen L, Pan K, Thomsen C (2018) Two-step process: enhanced strategy for wastewater treatment using microalgae. Bioresour Technol 268:608–615. https://doi.org/10.1016/j.biortech.2018.08.054

    Article  CAS  PubMed  Google Scholar 

  9. Chang JS (2018) Microalgae-based wastewater treatment and circular economy. New Biotechnol 44:S162–S162. https://doi.org/10.1016/j.nbt.2018.05.1178

    Article  Google Scholar 

  10. 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

    Article  CAS  Google Scholar 

  11. Serejo ML, Posadas E, Boncz MA, Blanco S, Garcia-Encina P, Munoz R (2015) Influence of biogas flow rate on biomass composition during the optimization of biogas upgrading in microalgal-bacterial processes. Environ Sci Technol 49(5):3228–3236. https://doi.org/10.1021/es5056116

    Article  CAS  PubMed  Google Scholar 

  12. Coppens J, Lindeboom R, Muys M, Coessens W, Alloul A, Meerbergen K, Lievens B, Clauwaert P, Boon N, Vlaeminck SE (2016) Nitrification and microalgae cultivation for two-stage biological nutrient valorization from source separated urine. Bioresour Technol 211:41–50. https://doi.org/10.1016/j.biortech.2016.03.001

    Article  CAS  PubMed  Google Scholar 

  13. Praveen P, Guo YC, Kang H, Lefebvre C, Loh KC (2018) Enhancing microalgae cultivation in anaerobic digestate through nitrification. Chem Eng J 354:905–912. https://doi.org/10.1016/j.cej.2018.08.099

    Article  CAS  Google Scholar 

  14. Nguyen TDP, Le TVA, Show PL, Nguyen TT, Tran MH, Tran TNT, Lee SY (2019) Bioflocculation formation of microalgae-bacteria in enhancing microalgae harvesting and nutrient removal from wastewater effluent. Bioresour Technol 272:34–39. https://doi.org/10.1016/j.biortech.2018.09.146

    Article  CAS  PubMed  Google Scholar 

  15. Qin L, Wang Z, Sun Y, Shu Q, Feng P, Zhu L, Xu J, Yuan Z (2016) Microalgae consortia cultivation in dairy wastewater to improve the potential of nutrient removal and biodiesel feedstock production. Environ Sci Pollut Res Int 23(9):8379–8387. https://doi.org/10.1007/s11356-015-6004-3

    Article  CAS  PubMed  Google Scholar 

  16. Li Y, Sun Y, Li L, Yuan Z (2018) Acclimation of acid-tolerant methanogenic propionate-utilizing culture and microbial community dissecting. Bioresour Technol 250:117–123. https://doi.org/10.1016/j.biortech.2017.11.034

    Article  CAS  PubMed  Google Scholar 

  17. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37(Database issue):D141-145. https://doi.org/10.1093/nar/gkn879

    Article  CAS  PubMed  Google Scholar 

  18. Li Y, Sun Y, Yang G, Hu K, Lv P, Li L (2017) Vertical distribution of microbial community and metabolic pathway in a methanogenic propionate degradation bioreactor. Bioresour Technol 245(Pt A):1022–1029. https://doi.org/10.1016/j.biortech.2017.09.028

    Article  CAS  PubMed  Google Scholar 

  19. Zhu S, Qin L, Feng P, Shang C, Wang Z, Yuan Z (2019) Treatment of low C/N ratio wastewater and biomass production using co-culture of Chlorella vulgaris and activated sludge in a batch photobioreactor. Bioresour Technol 274:313–320. https://doi.org/10.1016/j.biortech.2018.10.034

    Article  CAS  PubMed  Google Scholar 

  20. Qin L, Liu L, Wang Z, Chen W, Wei D (2018) Efficient resource recycling from liquid digestate by microalgae-yeast mixed culture and the assessment of key gene transcription related to nitrogen assimilation in microalgae. Bioresour Technol 264:90–97. https://doi.org/10.1016/j.biortech.2018.05.061

    Article  CAS  PubMed  Google Scholar 

  21. Rajagopal R, Masse DI, Singh G (2013) A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresour Technol 143:632–641. https://doi.org/10.1016/j.biortech.2013.06.030

    Article  CAS  PubMed  Google Scholar 

  22. Akerstrom AM, Mortensen LM, Rusten B, Gislerod HR (2014) Biomass production and nutrient removal by Chlorella sp. as affected by sludge liquor concentration. J Environ Manag 144:118–124. https://doi.org/10.1016/j.jenvman.2014.05.015

    Article  CAS  Google Scholar 

  23. de Morais MG, Costa JAV (2007) Biofixation of carbon dioxide by Spirulina sp. and Scenedesmus obliquus cultivated in a three-stage serial tubular photobioreactor. J Biotechnol 129(3):439–445. https://doi.org/10.1016/j.jbiotec.2007.01.009

    Article  CAS  PubMed  Google Scholar 

  24. Kim HS, Park WK, Lee B, Seon G, Suh WI, Moon M, Chang YK (2019) Optimization of heterotrophic cultivation of Chlorella sp. HS2 using screening, statistical assessment, and validation. Sci Rep. https://doi.org/10.1038/S41598-019-55854-9

    Article  PubMed  PubMed Central  Google Scholar 

  25. Summerfelt ST, Zuhlke A, Kolarevic J, Reiten BKM, Selset R, Gutierrez X, Terjesen BF (2015) Effects of alkalinity on ammonia removal, carbon dioxide stripping, and system pH in semi-commercial scale water recirculating aquaculture systems operated with moving bed bioreactors. Aquacult Eng 65:46–54. https://doi.org/10.1016/j.aquaeng.2014.11.002

    Article  Google Scholar 

  26. Peccia J, Haznedaroglu B, Gutierrez J, Zimmerman JB (2013) Nitrogen supply is an important driver of sustainable microalgae biofuel production. Trends Biotechnol 31(3):134–138. https://doi.org/10.1016/j.tibtech.2013.01.010

    Article  CAS  PubMed  Google Scholar 

  27. Lee J, Cho DH, Ramanan R, Kim BH, Oh HM, Kim HS (2013) Microalgae-associated bacteria play a key role in the flocculation of Chlorella vulgaris. Bioresour Technol 131:195–201. https://doi.org/10.1016/j.biortech.2012.11.130

    Article  CAS  PubMed  Google Scholar 

  28. Heylen K, Vanparys B, Peirsegaele F, Lebbe L, De Vos P (2007) Stenotrophomonas terrae sp. nov. and Stenotrophomonas humi sp. nov., two nitrate-reducing bacteria isolated from soil. Int J Syst Evol Microbiol 57(Pt 9):2056–2061. https://doi.org/10.1099/ijs.0.65044-0

    Article  CAS  PubMed  Google Scholar 

  29. Yu L, Liu Y, Wang G (2009) Identification of novel denitrifying bacteria Stenotrophomonas sp. ZZ15 and Oceanimonas sp. YC13 and application for removal of nitrate from industrial wastewater. Biodegradation 20(3):391–400. https://doi.org/10.1007/s10532-008-9230-2

    Article  CAS  PubMed  Google Scholar 

  30. Ren Y-X, Yang L, Liang X (2014) The characteristics of a novel heterotrophic nitrifying and aerobic denitrifying bacterium, Acinetobacter junii YB. Bioresour Technol 171:1–9. https://doi.org/10.1016/j.biortech.2014.08.058

    Article  CAS  PubMed  Google Scholar 

  31. Su JF, Zhang K, Huang TL, Wen G, Guo L, Yang SF (2015) Heterotrophic nitrification and aerobic denitrification at low nutrient conditions by a newly isolated bacterium, Acinetobacter sp. SYF26. Microbiology 161(Pt 4):829–837. https://doi.org/10.1099/mic.0.000047

    Article  CAS  PubMed  Google Scholar 

  32. He T, Li Z, Sun Q, Xu Y, Ye Q (2016) Heterotrophic nitrification and aerobic denitrification by Pseudomonas tolaasii Y-11 without nitrite accumulation during nitrogen conversion. Bioresour Technol 200:493–499. https://doi.org/10.1016/j.biortech.2015.10.064

    Article  CAS  PubMed  Google Scholar 

  33. Li C, Yang J, Wang X, Wang E, Li B, He R, Yuan H (2015) Removal of nitrogen by heterotrophic nitrification–aerobic denitrification of a phosphate accumulating bacterium Pseudomonas stutzeri YG-24. Bioresour Technol 182:18–25. https://doi.org/10.1016/j.biortech.2015.01.100

    Article  CAS  PubMed  Google Scholar 

  34. Heylen K, Lebbe L, De Vos P (2008) Acidovorax caeni sp. nov., a denitrifying species with genetically diverse isolates from activated sludge. Int J Syst Evol Microbiol 58(Pt 1):73–77. https://doi.org/10.1099/ijs.0.65387-0

    Article  CAS  PubMed  Google Scholar 

  35. Chakraborty P, Sarker RK, Roy R, Ghosh A, Maiti D, Tribedi P (2019) Bioaugmentation of soil with Enterobacter cloacae AKS7 enhances soil nitrogen content and boosts soil microbial functional-diversity. 3 Biotech 9(7):253. https://doi.org/10.1007/s13205-019-1791-8

    Article  PubMed  PubMed Central  Google Scholar 

  36. Tian HL, Zhao JY, Zhang HY, Chi CQ, Li BA, Wu XL (2015) Bacterial community shift along with the changes in operational conditions in a membrane-aerated biofilm reactor. Appl Microbiol Biotechnol 99(7):3279–3290. https://doi.org/10.1007/s00253-014-6204-7

    Article  CAS  PubMed  Google Scholar 

  37. Chen Q, Ni J (2011) Heterotrophic nitrification-aerobic denitrification by novel isolated bacteria. J Ind Microbiol Biotechnol 38(9):1305–1310. https://doi.org/10.1007/s10295-010-0911-6

    Article  CAS  PubMed  Google Scholar 

  38. Wang H, Song Q, Wang J, Zhang H, He Q, Zhang W, Song J, Zhou J, Li H (2018) Simultaneous nitrification, denitrification and phosphorus removal in an aerobic granular sludge sequencing batch reactor with high dissolved oxygen: effects of carbon to nitrogen ratios. Sci Total Environ 642:1145–1152. https://doi.org/10.1016/j.scitotenv.2018.06.081

    Article  CAS  PubMed  Google Scholar 

  39. Young S (2001) Pulp mill effluent induced coagulation and flocculation in receiving waters [D]. University of Alberta (Canada). https://doi.org/10.7939/R34Q7QR7X

  40. Dertli E, Mayer MJ, Narbad A (2015) Impact of the exopolysaccharide layer on biofilms, adhesion and resistance to stress in Lactobacillus johnsonii FI9785. BMC Microbiol 15:8. https://doi.org/10.1186/s12866-015-0347-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Jimenez JA, La Motta EJ, Parker DS (2007) Effect of operational parameters on the removal of particulate chemical oxygen demand in the activated sludge process. Water Environ Res 79(9):984–990. https://doi.org/10.2175/106143007x175717

    Article  CAS  PubMed  Google Scholar 

  42. More TT, Yadav JS, Yan S, Tyagi RD, Surampalli RY (2014) Extracellular polymeric substances of bacteria and their potential environmental applications. J Environ Manag 144:1–25. https://doi.org/10.1016/j.jenvman.2014.05.010

    Article  CAS  Google Scholar 

  43. Alleman JE, Preston K (1991) Behavior and physiology of nitrifying bacteria. In: Proceedings of the second annual conference on commercial

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Funding

This work was supported by the National Natural Science Foundation of China (51861145103 and 21878291); the Science and Technology Planning Project of Guangzhou (202102080406); the Natural Science Foundation for Research Team of Guangdong Province (2016A030312007).

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Authors and Affiliations

  1. Guangzhou Institute of Energy Conversion, Chinese Academy of Sciences, CAS Key Laboratory of Renewable Energy, Guangdong Provincial Key Laboratory of New and Renewable Energy Research and Development, Guangzhou, 510640, China

    Lei Qin, Siran Feng, Pinzhong Feng, Zhongming Wang & Shunni Zhu

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  1. Lei Qin
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  2. Siran Feng
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  3. Pinzhong Feng
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  4. Zhongming Wang
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  5. Shunni Zhu
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Contributions

LQ and SF carried out the experiments and wrote the manuscript. PF analyzed the data. ZW and SZ supervised the experimental work and revised the manuscript.

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Correspondence to Lei Qin or Shunni Zhu.

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Qin, L., Feng, S., Feng, P. et al. Treatment of Synthetic Ammonium Sulfate Wastewater by Mixed Culture of Chlorella pyrenoidosa and Enriched Nitrobacteria. Curr Microbiol 78, 3891–3900 (2021). https://doi.org/10.1007/s00284-021-02646-y

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