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Ammonium removal characteristics of heterotrophic nitrifying bacterium Pseudomonas stutzeri GEP-01 with potential for treatment of ammonium-rich wastewater

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Abstract

A heterotrophic nitrifying bacterium was isolated from the activated sludge and identified as Pseudomonas stutzeri GEP-01. Strain GEP-01 exhibited an efficient heterotrophic nitrification capability and a high nitrogen utilization rate, 48 mg/L NH4+-N was removed after culturing for 24 h without NO2−-N or NO3−-N accumulation, and 64.7% of the NH4+-N was removed by heterotrophic nitrification. Single-factor experiments indicated that factors such as the carbon source, temperature, NH4+-N load, and inoculum size had significant effects on the ammonium removal efficiency of strain GEP-01. The preferred conditions for heterotrophic nitrification were sodium citrate, 30 °C, 40 mg/L NH4+-N, and 5% inoculum size. When the initial NH4+-N amounts were 100, 200, 500 and 1000 mg/L, the removal rates were approximately 100%, 93%, 90.4%, and 78.9%, respectively, and higher ammonium concentrations require longer culture time. Nitrogen balance demonstrated that 40% of the initial nitrogen was lost, which was probably removed in the form of gas products under optimum culture conditions, and 36.3% of NH4+-N was converted to biomass. When incubated (adding a small amount of sodium citrate as carbon source and no carbon source) in swine wastewater containing 835 mg/L of ammonium, the removal ratio reached 56.3% and 24.8%. Strain GEP-01 has potential applications in the treatment of ammonium-rich wastewater.

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References

  1. Gao G, Clare AS, Rose C, Caldwell GS (2017) Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Mar Pollut Bull 114(1):439–447

    Article  CAS  Google Scholar 

  2. Xiang Y, Xiang Y, Wang L, Jiao Y (2018) Effects of coking wastewater on the growth of five wetland plant species. Bull Environ Contam Toxicol 100(2):265–270

    Article  CAS  Google Scholar 

  3. Cao L, Wang J, Xiang S, Huang Z, Ruan R, Liu Y (2019) Nutrient removal from digested swine wastewater by combining ammonia stripping with struvite precipitation. Environ Sci Pollut Res 26(7):6725–6734

    Article  CAS  Google Scholar 

  4. Wang S, Wu X, Wang Y, Li Q, Tao M (2008) Removal of organic matter and ammonia nitrogen from landfill leachate by ultrasound. Ultrason Sonochem 15(6):933–937

    Article  CAS  Google Scholar 

  5. Le C, Zha Y, Li Y, Sun D, Lu H, Yin B (2010) Eutrophication of lake waters in China: cost, causes, and control. Environ Manag 45(4):662–668

    Article  CAS  Google Scholar 

  6. Wang J, Fu Z, Qiao H, Liu F (2019) Assessment of eutrophication and water quality in the estuarine area of Lake Wuli, Lake Taihu, China. Sci Total Environ 650:1392–1402

    Article  CAS  Google Scholar 

  7. Hu J, Zhang G, Li K, Pa P, Chivas AR (2008) Increased eutrophication offshore Hong Kong, China during the past 75 years: evidence from high-resolution sedimentary records. Mar Chem 110(1–2):7–17

    Article  CAS  Google Scholar 

  8. Wang B, Xin M, Wei Q, Xie L (2018) A historical overview of coastal eutrophication in the China Seas. Mar Pollut Bull 136:394–400

    Article  CAS  Google Scholar 

  9. Gao F, Liao S, Liu S, Bai H, Wang A, Ye J (2019) The combination use of Candida tropicalis HH8 and Pseudomonas stutzeri LZX301 on nitrogen removal, biofloc formation and microbial communities in aquaculture. Aquaculture 500:50–56

    Article  CAS  Google Scholar 

  10. Shoda M, Ishikawa Y (2014) Heterotrophic nitrification and aerobic denitrification of high-strength ammonium in anaerobically digested sludge by Alcaligenes faecalis strain no. 4. J Biosci Bioeng 117(6):737–741

    Article  CAS  Google Scholar 

  11. Guo L, Chen Q, Fang F, Hu Z, Wu J, Miao A, Xiao L, Chen X, Yang L (2013) Application potential of a newly isolated indigenous aerobic denitrifier for nitrate and ammonium removal of eutrophic lake water. Biores Technol 142:45–51

    Article  CAS  Google Scholar 

  12. Yao S, Ni J, Chen Q, Borthwick AGL (2013) Enrichment and characterization of a bacteria consortium capable of heterotrophic nitrification and aerobic denitrification at low temperature. Biores Technol 127:151–157

    Article  CAS  Google Scholar 

  13. Zhang J, Wu P, Hao B, Yu Z (2011) Heterotrophic nitrification and aerobic denitrification by the bacterium Pseudomonas stutzeri YZN-001. Biores Technol 102(21):9866–9869

    Article  CAS  Google Scholar 

  14. Zhao B, Ran XC, Tian M, An Q, Guo JS (2018) Assessing the performance of a sequencing batch biofilm reactor bioaugmented with P. stutzeri strain XL-2 treating ammonium-rich wastewater. Biores Technol 270:70–79

    Article  CAS  Google Scholar 

  15. Zhou M, Ye H, Zhao X (2015) Ammonium removal by a novel heterotrophic nitrifying and aerobic denitrifying bacterium Pseudomonas stutzeri KTB from wastewater. Water Qual Res J Can 50(3):219–227

    Article  CAS  Google Scholar 

  16. Ji B, Wang H, Yang K (2014) Tolerance of an aerobic denitrifier (Pseudomonas stutzeri) to high O-2 concentrations. Biotechnol Lett 36(4):719–722

    Article  CAS  Google Scholar 

  17. Qing H, Donde OO, Tian C, Wang C, Wu X, Feng S, Liu Y, Xiao B (2018) Novel heterotrophic nitrogen removal and assimilation characteristic of the newly isolated bacterium Pseudomonas stutzeri AD-1. J Biosci Bioeng 126(3):339–345

    Article  CAS  Google Scholar 

  18. Sun Y, Li A, Zhang X, Ma F (2015) Regulation of dissolved oxygen from accumulated nitrite during the heterotrophic nitrification and aerobic denitrification of Pseudomonas stutzeri T13. Appl Microbiol Biotechnol 99(7):3243–3248

    Article  CAS  Google Scholar 

  19. Ueda A, Saneoka H (2015) Characterization of the ability to form biofilms by plant-associated Pseudomonas species. Curr Microbiol 70(4):506–513

    Article  CAS  Google Scholar 

  20. Sun Y, Feng L, Li A, Zhang X, Yang J, Ma F (2017) Ammonium assimilation: an important accessory during aerobic denitrification of Pseudomonas stutzeri T13. Biores Technol 234:264–272

    Article  CAS  Google Scholar 

  21. Frear D, Burrell R (1955) Spectrophotometric method for determining hydroxylamine reductase activity in higher plants. Anal Chem 27:1664–1665

    Article  CAS  Google Scholar 

  22. Kariminiaae-Hamedaani HR, Kanda K, Kato F (2004) Denitrification activity of the bacterium Pseudomonas sp ASM-2-3 isolated from the Ariake Sea tideland. J Biosci Bioeng 97(1):39–44

    Article  CAS  Google Scholar 

  23. 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. Biores Technol 182:18–25

    Article  CAS  Google Scholar 

  24. Yang L, Wang X-H, Cui S, Ren Y-X, Yu J, Chen N, Xiao Q, Guo L-K, Wang R-H (2019) Simultaneous removal of nitrogen and phosphorous by heterotrophic nitrification-aerobic denitrification of a metal resistant bacterium Pseudomonas putida strain NP5. Bioresour Technol 285:121360

    Article  CAS  Google Scholar 

  25. Chen S, He S, Wu C, Du D (2019) Characteristics of heterotrophic nitrification and aerobic denitrification bacterium Acinetobacter sp. T1 and its application for pig farm wastewater treatment. J Biosci Bioeng 127(2):201–205

    Article  CAS  Google Scholar 

  26. Zhao B, An Q, He YL, Guo JS (2012) N2O and N-2 production during heterotrophic nitrification by Alcaligenes faecalis strain NR. Biores Technol 116:379–385

    Article  CAS  Google Scholar 

  27. Zhao B, He YL, Zhang XF (2010) Nitrogen removal capability through simultaneous heterotrophic nitrification and aerobic denitrification by Bacillus sp LY. Environ Technol 31(4):409–416

    Article  CAS  Google Scholar 

  28. Sun Z, Lv Y, Liu Y, Ren R (2016) Removal of nitrogen by heterotrophic nitrification-aerobic denitrification of a novel metal resistant bacterium Cupriavidus sp S1. Biores Technol 220:142–150

    Article  CAS  Google Scholar 

  29. Liu Y, Ai G-M, Miao L-L, Liu Z-P (2016) Marinobacter strain NNA5, a newly isolated and highly efficient aerobic denitrifier with zero N2O emission. Biores Technol 206:9–15

    Article  CAS  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. Biores Technol 171:1–9

    Article  CAS  Google Scholar 

  31. Rout PR, Dash RR, Bhunia P, Rao S (2018) Role of Bacillus cereus GS-5 strain on simultaneous nitrogen and phosphorous removal from domestic wastewater in an inventive single unit multi-layer packed bed bioreactor. Biores Technol 262:251–260

    Article  CAS  Google Scholar 

  32. Krishna C, Van Loosdrecht MCM (1999) Effect of temperature on storage polymers and settleability of activated sludge. Water Res 33(10):2374–2382

    Article  CAS  Google Scholar 

  33. Chen Q, Ni JR (2012) Ammonium removal by Agrobacterium sp LAD9 capable of heterotrophic nitrification-aerobic denitrification. J Biosci Bioeng 113(5):619–623. https://doi.org/10.1016/j.jbiosc.2011.12.012

    Article  CAS  PubMed  Google Scholar 

  34. Lei Y, Wang Y, Liu H, Xi C, Song L (2016) A novel heterotrophic nitrifying and aerobic denitrifying bacterium, Zobellella taiwanensis DN-7, can remove high-strength ammonium. Appl Microbiol Biotechnol 100(9):4219–4229. https://doi.org/10.1007/s00253-016-7290-5

    Article  CAS  PubMed  Google Scholar 

  35. Yu Y, An Q, Zhou Y, Deng S, Miao Y, Zhao B, Yang L (2019) Highly synergistic effects on ammonium removal by the co-system of Pseudomonas stutzeri XL-2 and modified walnut shell biochar. Biores Technol 280:239–246

    Article  CAS  Google Scholar 

  36. Chen M, Wang W, Feng Y, Zhu X, Zhou H, Tan Z, Li X (2014) Impact resistance of different factors on ammonia removal by heterotrophic nitrification-aerobic denitrification bacterium Aeromonas sp HN-02. Biores Technol 167:456–461

    Article  CAS  Google Scholar 

  37. Vadivelu VM, Keller J, Yuan Z (2007) Effect of free ammonia on the respiration and growth processes of an enriched Nitrobacter culture. Water Res 41(4):826–834

    Article  CAS  Google Scholar 

  38. Anthonisen AC (1976) Inhibition of nitrification by ammonia and nitrous acid. J Water Pollut Control Fed 48:835–852

    CAS  PubMed  Google Scholar 

  39. Batchelor SE, Cooper M, Chhabra SR, Glover LA, Stewart GS, Williams P, Prosser JI (1997) Cell density-regulated recovery of starved biofilm populations of ammonia-oxidizing bacteria. Appl Environ Microbiol 63(6):2281–2286

    Article  CAS  Google Scholar 

  40. Ramadan MA, El-Tayeb OM, Alexander M (1990) Inoculum size as a factor limiting success of inoculum for biodegradation. Appl Environ Microbiol 56(5):1392–1396

    Article  CAS  Google Scholar 

  41. Jolliffe LK, Doyle RJ, Streips UN (1981) The energized membrane and cellular autolysis in Bacillus subtilis. Cell 25(3):753–763

    Article  CAS  Google Scholar 

  42. Zhang D, Li W, Huang X, Qin W, Liu M (2013) Removal of ammonium in surface water at low temperature by a newly isolated Microbacterium sp strain SFA13. Biores Technol 137:147–152

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Key R&D and Promotion Project of Henan Province (No. 192102310498); the Major Special Science and Technology Project of Henan Province (No. 181100310300); the National Science and Technology Major Project (No. 2017ZX07602-003-002); and the Key Scientific Research Project Plan of Colleges and Universities in Henan Province (No. 19B180012).

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Authors and Affiliations

  1. School of Water Conservancy Engineering, Zhengzhou University, Zhengzhou, 450001, People’s Republic of China

    Jingqing Gao, Tongdou Zhu, Chun Liu, Jingshen Zhang & Jianlei Gao

  2. Zhengzhou Yuanzhihe Environmental Protection Technology Co., Ltd., Zhengzhou, 450000, People’s Republic of China

    Jingshen Zhang

  3. Yellow River Engineering Consulting Co., Ltd., Zhengzhou, 450003, People’s Republic of China

    Jinliang Zhang & Ming Cai

  4. School of Pharmaceutical Sciences, Zhengzhou University, Zhengzhou, 450001, People’s Republic of China

    Yonghong Li

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  1. Jingqing Gao
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Gao, J., Zhu, T., Liu, C. et al. Ammonium removal characteristics of heterotrophic nitrifying bacterium Pseudomonas stutzeri GEP-01 with potential for treatment of ammonium-rich wastewater. Bioprocess Biosyst Eng 43, 959–969 (2020). https://doi.org/10.1007/s00449-020-02292-x

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