Skip to main content
SpringerLink
Log in

Kinetics of nitrate and sulfate removal using a mixed microbial culture with or without limited-oxygen fed

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The biological degradation of nitrate and sulfate was investigated using a mixed microbial culture and lactate as the carbon source, with or without limited-oxygen fed. It was found that sulfate reduction was slightly inhibited by nitrate, since after nitrate depletion the sulfate reduction rate increased from 0.37 mg SO4 2−/mg VSS d to 0.71 mg SO4 2−/mg VSS d, and the maximum rate of sulfate reduction in the presence of nitrate corresponded to 56 % of the non-inhibited sulfate reduction rate determined after nitrate depleted. However, simultaneous but not sequential reduction of both oxy-anions was observed in this study, unlike some literature reports in which sulfate reduction starts only after depletion of nitrate, and this case might be due to the fact that lactate was always kept above the limiting conditions. At limited oxygen, the inhibited effect on sulfate reduction by nitrate was relieved, and the sulfate reduction rate seemed relatively higher than that obtained without limited-oxygen fed, whereas kept almost constant (0.86–0.89 mg SO4 2−/mg VSS d) cross the six ROS states. In contrast, nitrate reduction rates decreased substantially with the increase in the initial limited-oxygen fed, showing an inhibited effect on nitrate reduction by oxygen. Kinetic parameters determined for the mixed microbial culture showed that the maximum specific sulfate utilization rate obtained (0.098 ± 0.022 mg SO4 2−/(mg VSS h)) was similar to the reported typical value (0.1 mg SO4 2−/(mg VSS h)), also indicating a moderate inhibited effect by nitrate.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Reference

  • American Public Health Association, American Water Works Association & Water Pollution Control Federation (APHA, AWWA & WPCF) (1995) Standard methods for the examination of water and wastewater. In: Eaton AD, Clesceri LS, Greenberg AE (Eds.), Standard methods for the examination of water and wastewater. Port City, Baltimore

  • An SJ, Stone H, Nemati M (2011) Biological removal of nitrate by an oil reservoir culture capable of autotrophic and heterotrophic activities: kinetic evaluation and modeling of the heterotrophic process. J Hazard Mater 190:686–693

    Article  CAS  PubMed  Google Scholar 

  • Bell LC, Richardson DJ, Ferguson SJ (1990) Periplasmic and membrane-bound respiratory nitrate reductases in Thiosphaera pantotropha. FEMS Lett 265:85–87

    Google Scholar 

  • Celis-Garcia LB, Gonzalez-Blanco G, Meraz M (2008) Removal of sulfur inorganic compounds by a biofilm of sulfate reducing and sulfide oxidizing bacteria in a down-flow fluidized bed reactor. J Chem Technol Biotechnol 83:260–268

    Article  CAS  Google Scholar 

  • Chen YR, Hashimoto AG (1980) Substrate utilization kinetic model for biological treatment processes. Biotechnol Bioeng 22:2081–2095

    Article  CAS  Google Scholar 

  • Chen C, Ren NQ, Wang AJ, Yu ZG, Lee DJ (2008) Microbial community of granules in expanded granular sludge bed reactor for simultaneous biological removal of sulfate, nitrate and lactate. Appl Microbiol Biotechnol 79:1071–1077

    Article  CAS  PubMed  Google Scholar 

  • Dannenberg S, Kroder M, Dilling W, Cypionka H (1992) Oxidation of H2, organic compounds and inorganic sulfur compounds coupled to reduction of O2 or nitrate by sulfate-reducing bacteria. Arch Microbiol 158:93–99

    Article  CAS  Google Scholar 

  • European Community (EC) (1980) Council directive of 15 July 1980 relating to the quality of water intended for human consumption. Off J Eur Commun 23(L229):11

    Google Scholar 

  • Gal H, Ronen Z, Weisbrod N, Dahan O, Ronit N (2008) Perchlorate biodegradation in contaminated soils and the deep unsaturated zone. Soil Biol Biochem 40:1751–1757

    Article  CAS  Google Scholar 

  • Garica de Lomas J, Corzo A, Gonzalez JM, Andrades JA, Iglesias E, Montero MJ (2006) Nitrate promotes biological oxidation of sulfide in wastewaters: experiment at plant-scale. Biotechnol Bioeng 93:801–811

    Article  Google Scholar 

  • Garcia de Lomas J, Corzo A, Portillo MC, Gonzalez JM, Andrades JA, Saiz-Jimenez C, Garcia-Robledo E (2007) Nitrate stimulation of indigenous nitrate-reducing, sulfide-oxidizing bacterial community in wastewater anaerobic biofilms. Water Res 41:3121–3131

    Article  CAS  PubMed  Google Scholar 

  • Gevertz D, Telang AJ, Voordouw G, Jenneman GE (2000) Isolation and characterization of strains of CVO and FWKO B. Two novel nitrate-reducing, sulfide-oxidizing bacteria isolated from oilfield brine. Appl Environ Microbiol 67:2491–2501

    Article  Google Scholar 

  • Greene EA, Hubert C, Nemati M, Jenneman GE, Voordouw G (2003) Nitrite reductase activity of sulfate-reducing bacteria prevents their inhibition by nitrate-reducing, sulfide-oxidizing bacteria. Environ Microbiol 5:607–617

    Article  CAS  PubMed  Google Scholar 

  • Hooijmans CM, Geraats SGM, van Neil EWJ, Robertson LA, Heijnen JJ, Luyben K (1990) Determination of growth and coupled nitrification/denitrification by immobilized Thiosphaera pantotropha using measurement and modeling of oxygen profiles. Biotechnol Bioeng 36:931–939

    Google Scholar 

  • Hubert C, Voordouw G (2007) Oil field souring control by nitrate-reducing Sulphurospirillum spp. that outcompete sulfate-reducing bacteria for organic electron donors. Appl Environ Microbiol 73:2644–2652

    Google Scholar 

  • Ingvorsen K, Zehnder AJB, Jorgensen BB (1984) Kinetics of sulfate uptake by Desulfobacter postgatei. Appl Environ Microbiol 47:403–408

    Google Scholar 

  • Johnston SL, Voordouw G (2012) Sulfate-reducing bacteria lower sulfur-mediated pitting corrosion under conditions of oxygen ingress. Environ Sci Technol 46:9183–9190

    Article  CAS  PubMed  Google Scholar 

  • Kaster KM, Grigoriyan A, Jenneman G, Voordouw G (2007) Effect of nitrate and nitrite on sulfide production by two thermophilic, sulfate-reducing enrichments from an oil field in the North Sea. Appl Microbiol Biotechnol 75:195–203

    Article  CAS  PubMed  Google Scholar 

  • Kelly DP, Wood AP (2000) Confirmation of Thiobacillus denitrificans as a species of genus Thiobacillus, in the β-subclass of the Proteobacteria, with strain NCIMB 9548 as the type strain. Int J Syst Evol Microbiol 50:547–550

    Google Scholar 

  • Klok JBM, van den Bosch PLF, Buisman CJN, Stams AJM, Keesman KJ, Janssen AJH (2012) Pathways of sulfide oxidation by haloalkaliphilic bacteria in limited-oxygen gas lift bioreactors. Environ Sci Technol 46:7581–7586

    Article  CAS  PubMed  Google Scholar 

  • Knowles R (1982) Denitrification. Microbiol Rev 46:43–70

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kornaros M, Lyberatos G (1998) Kinetic modeling of Pseudomonas denitrificans growth and denitrification under aerobic, anoxic and transient operating conditions. Water Res 32:1912–1922

    Google Scholar 

  • Matlab (2006) The Mathworks, Inc., Natick, MA, USA

  • Moosa S, Nemati M, Harrison STL (2002) A kinetic study on anaerobic reduction of sulfate, Part I: effect of sulfate concentration. Chem Eng Sci 57:2773–2780

    Article  CAS  Google Scholar 

  • Ni BJ, Ruscalleda M, Pellicer-Nacher C, Smets BF (2011) Modeling nitrous oxide production during biological nitrogen removal via nitrification and denitrification: extensions to the general ASM models. Environ Sci Technol 45:7768–7776

    Article  CAS  PubMed  Google Scholar 

  • Oh J, Silverstein J (1999) Oxygen inhibition of activated sludge denitrification. Water Res 33:1925–1937

    Article  CAS  Google Scholar 

  • Okabe S, Ito T, Sugita K, Satoh H (2005) Succession of internal sulfur cycles and sulfur-oxidizing bacterial communities in microaerophilic wastewater biofilms. Appl Environ Microbiol 71:2520–2529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Patureau D, Davison J, Bernet N, Moletta R (1994) Denitrification under various aeration conditions in Comamonas sp., strain SGLY 2. FEMS Microbiol Ecol 14:71–78

    Google Scholar 

  • Payne WJ (1973) Reduction of nitrogenous oxides by microorganisms. Bacteriol Rev 37:409–452

    CAS  PubMed Central  PubMed  Google Scholar 

  • Plosz BG, Jobbagy A, Grady CPL Jr (2003) Factors influencing deterioration of denitrification by oxygen entering an anoxic reactor through the surface. Water Res 37:853–863

    Article  CAS  PubMed  Google Scholar 

  • Reyes-Avila J, Razo-Flores E, Gomez J (2004) Simultaneous biological removal of nitrogen, carbon and sulfur by denitrification. Water Res 38:3313–3321

    Article  CAS  PubMed  Google Scholar 

  • Ricardo AR, Garvalho G, Velizarou S, Crespo JG, Reis MAM (2012) Kinetics of nitrate and perchlorate removal and biofilms stratification in an ion exchange membrane bioreactor. Water Res 46:4556–4568

    Article  CAS  PubMed  Google Scholar 

  • Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and application. McGraw-Hill Companies, Inc, New York

    Google Scholar 

  • Robertson LA, Kuenen JG (1984) Aerobic denitrification: a controversy revived. Arch Microbiol 139:351–354

    Article  CAS  Google Scholar 

  • Robertson LA, van Niel EWJ, Torremans RAM, Kuenen JG (1988) Simultaneous nitrification and denitrification in aerobic chemostat culture of Thiosphaera pantotropha. Appl Environ Microbiol 54:2812–2818

    Google Scholar 

  • Stouthamer AH (1988) Dissimilatory reduction of oxidized nitrogen compounds. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley & Sons, New York

    Google Scholar 

  • Tang Y, Ziv-El M, Zhou C, Shin JH, Ahn CH, Meyer K, Candelaria D, Friese D, Overstreet R, Scott R, Rittmann BE (2010) Bioreduction of nitrate in groundwater using a pilot-scale hydrogen-based membrane biofilm reactor. Front Environ Sci Eng China 4:280–285

    Article  CAS  Google Scholar 

  • Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. John Wiley & Sons, New York

    Google Scholar 

  • US Environmental Protection Agency (USEPA) (2010) National primary drinking water regulations; announcement of the results of EPA’s review of existing drinking water standards and request for public comment and/or information on related issues. Fed Regist 75(59):15500–15572

    Google Scholar 

  • US Environmental Protection Agency. Sulfate in drinking water. http://water.epa.gov/drink/contaminats/unregulated/sulfate.cfm. Accessed 7 Jun 2012

  • Valencia AO, Ziv-El M, Zhao HP, Feng L, Rittmann BE, Krajmalnik-Brown R (2012) Interactions between nitrate-reducing and sulfate-reducing bacteria coexisting in a hydrogen-fed biofilm. Environ Sci Technol 46:11289–11298

    Article  Google Scholar 

  • van den Ende FP, Meier J, van Gemerden H (1997) Syntrophic growth of sulfate-reducing bacteria and colorless sulfur bacteria during oxygen limitation. FEMS Microbiol Ecol 23:65–80

    Article  Google Scholar 

  • Vasiliadou IA, Pavlou S, Vayenas DV (2006) A kinetic study of hydrogenotrophic denitrification. Process Biochem 41:1401–1408

    Article  CAS  Google Scholar 

  • Visser A (1995) The anaerobic treatment of sulfate containing wastewater. Ph.D. thesis. Wageningen Argricultural University, Wageningen, The Netherlands

  • von Schulthess R, Gujer W (1996) Release of nitrous oxide (N2O) from denitrifying activated sludge: verification and application of a mathematical model. Water Res 30:521–530

    Article  Google Scholar 

  • Wu Q, Knowles R, Niven DF (1994) O2 regulation of denitrification in Flexibacter Canadensis. Can J Microbiol 40:916–921

    Article  CAS  Google Scholar 

  • Xu XJ, Chen C, Wang AJ, Fang N, Yuan Y, Ren NQ, Lee DJ (2012) Enhanced elementary sulfur recovery in integrated sulfate-reducing, sulfur-producing reactor under micro-aerobic condition. Bioresour Technol 116:517–521

    Article  CAS  PubMed  Google Scholar 

  • Xu XJ, Chen C, Lee DJ, Wang AJ, Guo WQ, Zhou X, Guo HL, Yuan Y, Ren NQ, Chang JS (2013) Sulfate-reduction, sulfide-oxidation and elemental sulfur bioreduction process: modeling and experimental validation. Bioresour Technol 147:202–211

    Article  CAS  PubMed  Google Scholar 

  • Zhang LH, De Schryver P, De Gusseme B, De Muynck W, Boon N, Verstrate W (2008) Chemical and biological technologies for hydrogen sulfide emission control in sewer systems: a review. Water Res 42:1–12

    Article  CAS  PubMed  Google Scholar 

  • Zhao HP, Valencia AO, Tang YN, Kim BO, Ilhan ZE, Krajmalnik-Brown R, Rittmann BE (2013) Using a two-stage hydrogen-based membrane biofilms reactor (MBfR) to achieve complete perchlorate reduction in the present of nitrate and sulfate. Environ Sci Technol 47:1565–1572

    CAS  PubMed  Google Scholar 

  • Ziv-El M, Rittmann BE (2009) Water-quality assessment after treatment in a membrane biofilms reactor. J Am Water Works Assoc 101(12):77–83

    CAS  Google Scholar 

  • Zumft WG (1992) The denitrifying prokaryotes. In: Balows AB, Truper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes. Springer-Verlag, New York, pp 554–582

    Google Scholar 

Download references

Acknowledgments

This research was supported by the National High-tech R&D Program of China (863 Program, Grant No. 2011AA060904), the National Natural Science Foundation of China (Grant Nos. 51176037 and 51308147), Project 51121062 (National Creative Research Groups), the State Key Laboratory of Urban Water Resource and Environment (2012DX06), and the Academician Workstation Construction in Guangdong Province (2012B090500018).

Author information

Authors and Affiliations

  1. State Key Laboratory of Urban Water Resource and Environment, School of Municipal and Environmental Engineering, Harbin Institute of Technology, P.O. Box 2650, 73 Huanghe Road, Nangang District, Harbin, 150090, Heilongjiang, China

    Xi-jun Xu, Chuan Chen, Ai-jie Wang, Hong-liang Guo, Ye Yuan, Duu-Jong Lee & Nan-qi Ren

  2. Department of Chemical Engineering, National Taiwan University, Taipei 106, Taiwan

    Duu-Jong Lee

Authors
  1. Xi-jun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chuan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ai-jie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hong-liang Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ye Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Duu-Jong Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nan-qi Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ai-jie Wang or Nan-qi Ren.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, Xj., Chen, C., Wang, Aj. et al. Kinetics of nitrate and sulfate removal using a mixed microbial culture with or without limited-oxygen fed. Appl Microbiol Biotechnol 98, 6115–6124 (2014). https://doi.org/10.1007/s00253-014-5642-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-5642-6

Keywords

Search

Navigation