Skip to main content

Advertisement

Log in

Novel approach for the ammonium removal by simultaneous heterotrophic nitrification and denitrification using a novel bacterial species co-culture

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Agricultural activities lead excessive emission of ammonia nitrogen in the environment and can profoundly interfere the equilibrium of the natural ecosystems leading to their contamination. Actually, the biological purification of wastewaters is the most adopted technique thanks to its several advantages such as high performance and low energy consumption. For this reason, two novel strains of Alcaligenes sp. S84S3 and Proteus sp. S19 genus were isolated from an activated sludge and applied in the treatment of ammonium and nitrite in aqueous solution. Under the optimum operating conditions of temperature (30 °C), pH (7), carbon substrate (2 g/L of glucose) and duration of incubation time (69 h), the strain Alcaligenes sp. S84S3 could oxidize 65 % of the ammonium as high as 272.72 mg-NH4 +/L. Moreover, during 48 h, the nitrate reduction rate performed by the strain Proteus S19 was about 99 % without production of nitrite intermediate (negligible concentration). Moreover, the coculture of the strains Alcaligenes sp. S84S3 and Proteus sp. S19 could eliminate 65.83 % of the ammonium ions without production of toxic forms of nitrogen oxides during a short time of incubation (118 h) at the same operational conditions with providing the aeration in the first treatment phase. The coculture of our isolated strains is assumed to have a good potential for nitrification and denitrification reactions applied in the treatment of wastewater containing ammonium, nitrite and nitrate. As a result, we can consider that the mixed culture is a practical method in the treatment of high-strength ammonium wastewater with reducing of sludge production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abo-Amer AE, El-Shanshoury AERR, Alzahrani OM (2015) Isolation and molecular characterization of heavy metal-resistant Alcaligenes faecalis from Sewage wastewater and synthesis of silver nan. Geomicrobiol J 32(9):836–845

    Article  CAS  Google Scholar 

  • American Public Health Association (2011) Standard methods for the examination of water and wastewater, 21st edn. American Waterworks Association and Water Pollution Control Federation, Baltimore

    Google Scholar 

  • Aurelio M, Briones Jr, Satoshi O, Yoshiaki U, Niels-Birger R, Wolfgang R, Hidetoshi O (2003) Ammonia-oxidizing bacteria on root biofilms and their possible contribution to N use efficiency of different rice cultivars. Plant Soil 250:335–348

    Article  Google Scholar 

  • Bouchotroch S, Quesada E, Del Moral A, Llamas I, Bejar V (2001) Halomonasmaura sp. nov., a novel moderately halophilic, exopolysaccharide-producing bacterium. Int J Syst Evol Microbiol 51:1625–1632

    Article  CAS  Google Scholar 

  • Briones AM Jr, Okabe S, Umemiya Y, Ramsing NB, Reichardt W, Okuyama H (2003) Ammonia-oxidizing bacteria on root biofilms and their possible contribution to N use efficiency of different rice cultivars. Plant Soil 250:335–348

    Article  CAS  Google Scholar 

  • Chen G, Cao X, Song C, Zhou Y (2010) Adverse effects of ammonia on nitrification process: the case of chinese shallow freshwater lakes. Water Air Soil Pollut 210:297–306

    Article  CAS  Google Scholar 

  • 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. Bioresour Technol 167:456–461

    Article  CAS  Google Scholar 

  • Cheng W, Tsuruta H, Chen G, Yagi K (2004) N2O and NO production in various Chinese agricultural soils by nitrification. Soil Biol Biochem 36:953–963

    Article  CAS  Google Scholar 

  • Converti A, Scapazzoni Lodi S, Carvalho JCM (2006) Ammonium and urea removal by Spirulina platensis. J Ind Microbiol Biotechnol 33:8–16

    Article  CAS  Google Scholar 

  • Czlircin E, Mtszhros-Kis A, Domokos E, Papp J (1988) Separation of ammonia from wastewater using clinoptilolite as ion exchanger. Nucl Chem Waste Manag 8:107–113

    Article  Google Scholar 

  • Dinçer AR, Kargı F (2000) Kinetics of sequential nitrification and denitrification processes. Enzyme Microb Technol 27:37–42

    Article  Google Scholar 

  • Du G, Geng J, Chen J, Lun S (2003) Mixed culture of nitrifying bacteria and denitrifying bacteria for simultaneous nitrification and denitrification. World J Microbiol Biotechnol 19:433–437

    Article  CAS  Google Scholar 

  • Fu Z, Zhao J (2015) Impact of quinoline on activity and microbial culture of partial nitrification process. Bioresour Technol 197:113–119

    Article  CAS  Google Scholar 

  • Ganiguéo R, Lôpez H, Balaguero MD, Colprim J (2007) Partial ammonium oxidation to nitrite of high ammonium content urban landfill leachates. Water Res 41:3317–3326

    Article  Google Scholar 

  • Gao D, Peng Y, Li B, Liang H (2009) Shortcut nitrification–denitrification by real-time control strategies. Bioresour Technol 100:2298–2300

    Article  CAS  Google Scholar 

  • Ge S, Wang S, Yang X, Qiu S, Li B, Peng Y (2015) Detection of nitrifiers and evaluation of partial nitrification for wastewater treatment. Chemosphere 140:85–98

    Article  CAS  Google Scholar 

  • Guo H, Zhou J, Su J, Zhang Z (2005) Integration of nitrification and denitrification in airlift bioreactor. Biochem Eng J 23:57–62

    Article  CAS  Google Scholar 

  • Gupta AB, Gupta SK (2001) Simultaneous carbon and nitrogen removal from high strength domestic wastewater in an aerobic RBC biofilm. Water Res 35(7):1714–1722

    Article  CAS  Google Scholar 

  • Hamoda MF, Zeidan MO, Haddad AA (1996) Biological nitrification kinetics in a fixed-film reactor. Bioresour Technol 58:41–48

    Article  CAS  Google Scholar 

  • Hawkins S, Robinson K, Layton A, Sayler G (2012) Molecular indicators of Nitrobacter spp. population and growth activity during an induced inhibition event in a bench scale nitrification reactor. Water Res 46:1793–1802

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Isaka K, Yoshie S, Sumino T, Inamori Y, Tsuneda S (2007) Nitrification of landfill leachate using immobilized nitrifying bacteria at low temperatures. Biochem Eng J 37:49–55

    Article  CAS  Google Scholar 

  • Joo HS, Hirai M, Shoda M (2005) Characteristics of ammonium removal by heterotrophic nitrification-aerobic denitrification by Alcaligenes faecalis No. 4. J Biosci Bioeng 100(2):184–191

    Article  CAS  Google Scholar 

  • Joo HS, Hirai M, Shoda M (2006) Piggery wastewater treatment using Alcaligenes faecalis strain No. 4 with heterotrophic nitrification and aerobic denitrification. Water Res 40:3029–3036

    Article  CAS  Google Scholar 

  • Kathiravan V, Krishnani KK (2014) Pseudomonasaeruginosa and Achromobactersp.: nitrifying aerobic denitrifiers have a plasmid encoding for denitrifying functional genes. World J Microbiol Biotechnol 30:1187–1198

    Article  CAS  Google Scholar 

  • Khanitchaidecha W, Sumino T, Kazama F (2010) Influence of carbon source on biological nitrogen removal by immobilised bacteria. J Water Resour Prot 2:527–531

    Article  CAS  Google Scholar 

  • Kim DJ, Lee DI, Keller J (2006) Effect of temperature and free ammonia on nitrification and nitrite accumulation in landfill leachate and analysis of its nitrifying bacterial community by FISH. Bioresour Technol 97:459–468

    Article  CAS  Google Scholar 

  • Li X, Lin C, Wang Y, Zhao M, Hou Y (2010) Clinoptilolite adsorption capability of ammonia in pig farm. Procedia Environ  Sci  2:1598–1612

    Article  Google Scholar 

  • Liang SC, Zhao M, Lu L, Wang CL, Zhao LY, Liu WJ (2011) Isolation and characteristic of an aerobic denitrifier with high nitrogen removal efficiency. Afr J Biotechnol 10(52):10648–10656

    CAS  Google Scholar 

  • Lin L, Lei Z, Wang L, Liu X, Zhang Y, Wan C, Lee DJ, Tay JH (2013) Adsorption mechanisms of high-levels of ammonium onto natural and NaCl-modified zeolites. Sepa Purifi Technol 103:15–20

    Article  CAS  Google Scholar 

  • Lin SH, Wu CL (1996) Removal of nitrogenous compounds from aqueous solution by ozonation and ion exchange. Wat Res 30(8):1851–1857

    Article  CAS  Google Scholar 

  • López-Legentil S, Erwin PM, Pawlik JR, Song B (2010) Effects of sponge bleaching on ammonia-oxidizing archaea: distribution and relative expression of ammonia monooxygenase genes associated with the barrel sponge Xestospongiamuta. Microbiol Ecolol 60:561–571

    Article  Google Scholar 

  • Morozkina EV, Zvyagilskaya RA (2007) Nitrate reductases: structure, functions, and effect of stress factors. Biochemistry (Moscow) 72(10):1151–1160

    Article  CAS  Google Scholar 

  • Nishio T, Yoshikura T, Mishima H, Inouye Z, Itoh H (1998) Conditions for nitrification and denitrification by an immobilized heterotrophic nitrifying bacterium alcaligenes faecalis OKK 17. J Ferment Bioeng 86(4):351–356

    Article  CAS  Google Scholar 

  • Oorts K, Merckx R, Ghan E, Labreuche J, Nicolardot B (2007) Determinants of annual fluxes of CO2 and N2O in long-term no-tillage and conventional tillage systems in northern France. Soil Tillage Res 95:133–148

    Article  Google Scholar 

  • Ozturk I, Altinbas M, Koyuncu I, Arikan O, Gomec-Yangin C (2003) Advanced physico-chemical treatment experiences on young municipal landfill leachates. Waste Manage 23:441–446

    Article  CAS  Google Scholar 

  • Pansu M, Thuries L (2003) Kinetics of C and N mineralization, N immobilization and N volatilization of organic inputs in soil. Soil Biol & Biochem 35:37–48

    Article  CAS  Google Scholar 

  • Rahman MM, Salleh MAM, Rashid U, Ahsan A, Hossain M, Chang Six Ra M (2014) Production of slow release crystal fertilizer from wastewaters through struvite crystallization. Arabian J Chem 7:139–155

    Article  CAS  Google Scholar 

  • Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsisrepresents a phylogenetically coherent taxon and a distinct actinomycete lineage; proposal of Nocardiopsaceae fam. Nov. Int J Syst Bacteriol 46:1088–1092

    Article  CAS  Google Scholar 

  • Rehfuss M, Urban J (2005) Alcaligenes faecalis subsp. Phenolicus subsp. nov. a phenol-degrading, denitrifying bacterium isolated from a gray water bioprocessor. Syst Appl Microbiol 28:421–429

    Article  CAS  Google Scholar 

  • Ruiz G, Jeison D, Rubilar O, Ciudad G, Chamy R (2006) Nitrification–denitrification via nitrite accumulation for nitrogen removal from wastewaters. Bioresour Technol 97:330–335

    Article  CAS  Google Scholar 

  • Shao MF, Zhang T, Han-Ping Fang H (2010) Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications. Appl Microbiol Biotechnol 88:1027–1042

    Article  CAS  Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Manual of methods for general microbiology. American Society for Microbiology, Washington, pp 611–654

    Google Scholar 

  • Sugiyama S, Yokoyama M, Ishizuka H, Sotowa KI, Tomida T, Shigemo N (2005) Removal of aqueous ammonium with magnesium phosphates obtained from the ammonium elimination of magnesium ammonium phosphate. Colloid Interface Sci 292:133–138

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  Google Scholar 

  • Valverde-Sarmiento C, Espinosa-Iglesias D, Bautista-Toledo I, Ivarez-Merino MA, Maldonado-Hodar FJ, Carrasco-Marin F, Pérez-Cadenas AF (2015) Bacteria supported on carbon films for water denitrification. Chem Eng J 259:424–429

    Article  CAS  Google Scholar 

  • Van Trappen S, Tan TL, Samyn E, Vandamme P (2005) Alcaligenesaquatilis sp. nov., a novel bacterium from sediments of the Weser Estuary, Germany, and a salt marsh on Shem Creek in Charleston Harbor, USA. Int J Syst Evol Microbiol 55:2571–2575

    Article  Google Scholar 

  • Verstraete W, Alexander M (1992) Heterotrophic Nitrification by Arthrobacter sp. J Bacteriol 110(3):955–961

    Google Scholar 

  • Wang J, Peng Y, Wang S, Gao Y (2008) Nitrogen removal by simultaneous nitrification and denitrification via nitrite in a sequence hybrid biological reactor. Chin J Chem Eng 16(5):778–784

    Article  CAS  Google Scholar 

  • Wang H, He J, Ma F, Yang K, Wei L (2011) Aerobic denitrification of a Pseudomonas sp. Isolated from a high strength ammonium wastewater treatment facility. J Scientific Res Essays 6(4):748–755

    CAS  Google Scholar 

  • Wen Y, Wei CH (2011) Heterotrophic nitrification and aerobic denitrification bacterium isolated from anaerobic/anoxic/oxic treatment system. Afr J Biotechnol 10(36):6985–6990

    CAS  Google Scholar 

  • Wu J, Xu T, Yan G, He C, Zhou G (2015) Model predictive control of partial nitrification via nitrous oxide (N2O) emission monitoring. J Environ Chem Eng 3:2857–2865

    Article  CAS  Google Scholar 

  • Xin X, Jiang X, Su J, Yan X, Ni J, Faeflen SJ, Huang X, Wright AL (2016) Manganese oxide affects nitrification and ammonia oxidizers in subtropical and temperate acid forest soils. Catena 137:24–30

    Article  CAS  Google Scholar 

  • Yao S, Ni J, Tao Ma T, Li C (2013) Heterotrophic nitrification and aerobic denitrification at low temperature by a newly isolated bacterium, Acinetobacter sp. HA2. Bioresour Technol 139:80–86

    Article  CAS  Google Scholar 

  • Yu R, Geng J, Ren H, Wang Y, Xu K (2013) Struvite pyrolysate recycling combined with dry pyrolysis for ammonium removal from wastewater. Bioresour Technol 132:154–159

    Article  CAS  Google Scholar 

  • Zhang T, Ye L, Hin A, Tong Y, Shao MF, Lok S (2011) Ammonia-oxidizing archaea and ammonia-oxidizing bacteria in six full-scale wastewater treatment bioreactors. Appl Microbiol Biotechnol 91:1215–1225

    Article  CAS  Google Scholar 

  • Zhang Y, Shi Z, Chen M, Dong X, Zhou J (2015) Evaluation of simultaneous nitrification and denitrification under controlled conditions by an aerobic denitrifier culture. Bioresour Technol 175:602–605

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Prof. Amina Khemili and Assia Benakouche for their careful reading.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yassmina Angar.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Angar, Y., Kebbouche-Gana, S., Djelali, NE. et al. Novel approach for the ammonium removal by simultaneous heterotrophic nitrification and denitrification using a novel bacterial species co-culture. World J Microbiol Biotechnol 32, 36 (2016). https://doi.org/10.1007/s11274-015-2007-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-015-2007-y

Keywords

Navigation