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References

  1. Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MCM. 2014. Full-scale partial nitritation/anammox experiences – an application survey. Water Res. 55: 292-303.
    Pubmed CrossRef
  2. Morales N, Val del Río Á, Vázquez-Padín JR, Méndez R, Mosquera-Corral A, Campos JL. 2015. Integration of the anammox process to the rejection water and main stream lines of WWTPs. Chemosphere 140: 99-105.
    Pubmed CrossRef
  3. Shi YJ, Wells G, Morgenroth E. 2016. Microbial activity balance in size fractionated suspended growth biomass from full-scale sidestream combined nitritation-anammox reactors. Bioresour. Technol. 218: 38-45.
    Pubmed CrossRef
  4. Strous M, Heijnen JJ, Kuenen JG, Jetten MSM. 1998. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Biochem. Biotechnol. 50: 589-596.
    CrossRef
  5. Sinha B, Annachhatre AP. 2006. Partial nitrification - operational parameters and microorganisms involved. Rev. Environ. Sci. Biotechnol. 6: 285-313.
    CrossRef
  6. Third KA, Sliekers AO, Kuenen JG, Jetten MS. 2001. The CANON system (Completely Autotrophic Nitrogen-removal Over Nitrite) under ammonium limitation: interaction and competition between three groups of bacteria. Syst. Appl. Microbiol. 24: 588-596.
    Pubmed CrossRef
  7. Wang L, Zheng P, Chen TT, Chen JW, Xing YJ, Ji QX, et al. 2012. Performance of autotrophic nitrogen removal in the granular sludge bed reactor. Bioresour. Technol. 123: 78-85.
    Pubmed CrossRef
  8. Varas R, Guzmán-Fierro V, Giustinianovich E, Behar J, Fernández K, Roeckel M. 2015. Startup and oxygen concentration effects in a continuous granular mixed flow autotrophic nitrogen removal reactor. Bioresour. Technol. 190: 345-351.
    Pubmed CrossRef
  9. Vázquez-Padín J, Mosquera-Corral A, Campos JL, Méndez R, Revsbech NP. 2010. Microbial community distribution and activity dynamics of granular biomass in a CANON reactor. Water Res. 44: 4359-4370.
    Pubmed CrossRef
  10. Vlaeminck SE, Terada A, Smets BF, De Clippeleir H, Schaubroeck T, Bolca S, et al. 2010. Aggregate size and architecture determine microbial activity balance for one-stage partial nitritation and anammox. Appl. Environ. Microbiol. 76: 900-909.
    Pubmed PMC CrossRef
  11. Volcke EI, Picioreanu C, De Baets B, van Loosdrecht MCM. 2012. The granule size distribution in an anammox-based granular sludge reactor affects the conversion - implications for modeling. Biotechnol. Bioeng. 109: 1629-1636.
    Pubmed CrossRef
  12. Lotti T, Kleerebezem R, Hu Z, Kartal B, Jetten MS, van Loosdrecht MCM. 2014. Simultaneous partial nitritation and anammox at low temperature with granular sludge. Water Res. 66: 111-121.
    Pubmed CrossRef
  13. Guo JH, P eng YZ, F an L , Zhang L, N i BJ, Kartal B , et al. 2016. Metagenomic analysis of anammox communities in three different microbial aggregates. Environ. Microbiol. 18: 2979-2993.
    Pubmed CrossRef
  14. Pérez J, Lotti T, Kleerebezem R, Picioreanu C, van Loosdrecht MCM. 2014. Outcompeting nitrite-oxidizing bacteria in single-stage nitrogen removal in sewage treatment plants:a model-based study. Water Res. 66: 208-218.
    Pubmed CrossRef
  15. Wang L, Zheng P, Xing YJ, Li W, Yang J, Abbas G, et al. 2014. Effect of particle size on the performance of autotrophic nitrogen removal in the granular sludge bed reactor and microbiological mechanisms. Bioresour. Technol. 157: 240-246.
    Pubmed CrossRef
  16. Qian FY, Wang JF, Shen YL, Wang Y, Wang SY, Chen X. 2017. Achieving high performance completely autotrophic nitrogen removal in a continuous granular sludge reactor. Biochem. Eng. J. 118: 97-104.
    CrossRef
  17. APHA. 1998. Standard Methods for Examination of Water and Wastewater, 20th Ed. American Public Health Association, Washington, DC, USA.
  18. Adav SS, Lee DJ. 2008. Extraction of extracellular polymeric substances from aerobic granule with compact interior structure. J. Hazard. Mater. 154: 1120-1126.
    Pubmed CrossRef
  19. Bassin JP, Kleerebezem R, Dezotti M, van Loosdrecht MCM. 2012. Measuring biomass specific ammonium, nitrite and phosphate uptake rates in aerobic granular sludge. Chemosphere 89: 1161-1168.
    Pubmed CrossRef
  20. Wang JF , Qian F Y, L iu XP, L iu W R, W ang SY, Shen Y L. 2016. Cultivation and characteristics of partial nitrification granular sludge in a sequencing batch reactor inoculated with heterotrophic granules. Appl. Microbiol. Biotechnol. 100:9381-9391.
    Pubmed CrossRef
  21. Ohene-Adjei S, Teather RM, Ivan M, Forster RJ. 2007. Postinoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Appl. Environ. Microbiol. 73: 4609-4618.
    Pubmed PMC CrossRef
  22. Stahl DA, de la Torre JR. 2012. Physiology and diversity of ammonia-oxidizing archaea. Annu. Rev. Microbiol. 66: 83-101.
    Pubmed CrossRef
  23. Vlaeminck SE, Terada A, Smets BF, van der Linden D, Boon N, Verstraete W, et al. 2009. Nitrogen removal from digested black water by one-stage partial nitritation and anammox. Environ. Sci. Technol. 43: 5035-5041.
    Pubmed CrossRef
  24. Lv YT, Wang L, Sun T, Wang XD, Yang YZ, Wang ZY. 2010. Autotrophic nitrogen removal discovered in suspended nitritation system. Chemosphere 79: 180-185.
    Pubmed CrossRef
  25. Winkler MK, Kleerebezem R, Kuenen JG, Yang J, van Loosdrecht MCM. 2011. Segregation of biomass in cyclic anaerobic/aerobic granular sludge allows the enrichment of anaerobic ammonium oxidizing bacteria at low temperatures. Environ. Sci. Technol. 45: 7330-7337.
    Pubmed CrossRef
  26. Verawaty M, Pijuan M, Yuan Z, Bond PL. 2012. Determining the mechanisms for aerobic granulation from mixed seed of floccular and crushed granules in activated sludge wastewater treatment. Water Res. 46: 761-771.
    Pubmed CrossRef
  27. Li XJ, Sun S, Badgley BD, Sung S, Zhang H, He Z. 2016. Nitrogen removal by granular nitritation-anammox in an upflow membrane-aerated biofilm reactor. Water Res. 94: 23-31.
    Pubmed CrossRef
  28. Li W, Zheng P, Ji JY, Zhang M, Guo J, Zhang JQ, et al. 2014. Floatation of granular sludge and its mechanism: a key approach for high-rate denitrifying reactor. Bioresour. Technol. 152: 414-419.
    Pubmed CrossRef
  29. Hubaux N, Wells G, Morgenroth E. 2015. Impact of coexistence of flocs and biofilm on performance of combined nitritationanammox granular sludge reactors. Water Res. 68: 127-139.
    Pubmed CrossRef
  30. Cho S, Fujii N, Lee T, Okabe S. 2011. Development of a simultaneous partial nitrification and anaerobic ammonia oxidation process in a single reactor. Bioresour. Technol. 102:652-659.
    Pubmed CrossRef
  31. Bartrolí A, Pérez J, Carrera J. 2010. Applying ratio control in a continuous granular reactor to achieve full nitritation under stable operating conditions. Environ. Sci. Technol. 44: 8930-8935.
    Pubmed CrossRef
  32. Tang CJ, Zheng P, Wang CH, Mahmood Q, Zhang JQ, Chen XG, et al. 2011. Performance of high-loaded ANAMMOX UASB reactors containing granular sludge. Water Res. 45: 135-144.
    Pubmed CrossRef
  33. Oshiki M, Satoh H, Okabe S. 2016. Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ. Microbiol. 18: 2784-2796.
    Pubmed CrossRef
  34. Ma B, Bao P, Wei Y, Zhu GB, Yuan ZG, Peng YZ. 2015. Suppressing nitrite-oxidizing bacteria growth to achieve nitrogen removal from domestic wastewater via anammox using intermittent aeration with low dissolved oxygen. Sci. Rep. 5: 13048-13057.
    Pubmed PMC CrossRef
  35. Wett B, Omari A, Podmirseg SM, Han M, Akinayo O, Gómez Brandón M, et al. 2013. Going for mainstream deammonification from bench to full scale for maximized resource efficiency. Water Sci. Technol. 68: 283-289.
    Pubmed CrossRef
  36. Regmi P, Mark WM, Holgate B, Bunce R, Park H, Chandran K, et al. 2014. Control of aeration, aerobic SRT and COD input for mainstream nitritation/denitritation. Water Res. 57: 162-171.
    Pubmed CrossRef
  37. Nowka B, Daims H, Spieck E. 2015. Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Appl. Environ. Microbiol. 81: 745-753.
    Pubmed PMC CrossRef
  38. Zhang L, Liu MM, Zhang SJ, Yang YD, Peng YZ. 2015. Integrated fixed-biofilm activated sludge reactor as a powerful tool to enrich anammox biofilm and granular sludge. Chemosphere 140: 114-118.
    Pubmed CrossRef
  39. Han M, Vlaeminck SE, Al-Omari A, Wett B, Bott C, Murthy S, et al. 2016. Uncoupling the solids retention times of flocs and granules in mainstream deammonification: a screen as effective out-selection tool for nitrite oxidizing bacteria. Bioresour. Technol. 221: 195-204.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(10): 1798-1807

Published online October 28, 2017 https://doi.org/10.4014/jmb.1705.05042

Copyright © The Korean Society for Microbiology and Biotechnology.

Differentiation in Nitrogen-Converting Activity and Microbial Community Structure between Granular Size Fractions in a Continuous Autotrophic Nitrogen Removal Reactor

Feiyue Qian 1, 2, Xi Chen 1, Jianfang Wang 1, 2*, Yaoliang Shen 1, 2, Junjun Gao 1 and Juan Mei 1, 2

1College of Environmental Science and Engineering, Suzhou University of Science and Technology, Suzhou 215009, P.R. China, 2National and Local Joint Engineering Laboratory of Municipal Sewage Resource Utilization Technology, Suzhou 215009, P.R. China

Received: May 16, 2017; Accepted: August 1, 2017

Abstract

The differentiations in nitrogen-converting activity and microbial community structure
between granular size fractions in a continuous completely autotrophic nitrogen removal over
nitrite (CANON) reactor, having a superior specific nitrogen removal rate of 0.24 g/(g VSS·d),
were investigated by batch tests and high-throughput pyrosequencing analysis, respectively.
Results revealed that a high dissolved oxygen concentration (>1.8 mg/l) could result in
efficient nitrite accumulation with small granules (0.2-0.6 mm in diameter), because aerobic
ammonium-oxidizing bacteria (genus Nitrosomonas) predominated therein. Meanwhile,
intermediate size granules (1.4-2.0 mm in diameter) showed the highest nitrogen removal
activity of 40.4 mg/(g VSS·h) under sufficient oxygen supply, corresponding to the relative
abundance ratio of aerobic to anaerobic ammonium-oxidizing bacteria (genus Candidatus
Kuenenia) of 5.7. Additionally, a dual substrate competition for oxygen and nitrite would be
considered as the main mechanism for repression of nitrite-oxidizing bacteria, and the few
Nitrospira spp. did not remarkably affect the overall performance of the reactor. Because all the
granular size fractions could accomplish the CANON process independently under oxygen
limiting conditions, maintaining a diversity of granular size would facilitate the stability of the
suspended growth CANON system.

Keywords: Aerobic granular sludge, autotrophic nitrogen removal, granular size fraction, dissolved oxygen condition, microbial community structure

References

  1. Lackner S, Gilbert EM, Vlaeminck SE, Joss A, Horn H, van Loosdrecht MCM. 2014. Full-scale partial nitritation/anammox experiences – an application survey. Water Res. 55: 292-303.
    Pubmed CrossRef
  2. Morales N, Val del Río Á, Vázquez-Padín JR, Méndez R, Mosquera-Corral A, Campos JL. 2015. Integration of the anammox process to the rejection water and main stream lines of WWTPs. Chemosphere 140: 99-105.
    Pubmed CrossRef
  3. Shi YJ, Wells G, Morgenroth E. 2016. Microbial activity balance in size fractionated suspended growth biomass from full-scale sidestream combined nitritation-anammox reactors. Bioresour. Technol. 218: 38-45.
    Pubmed CrossRef
  4. Strous M, Heijnen JJ, Kuenen JG, Jetten MSM. 1998. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Biochem. Biotechnol. 50: 589-596.
    CrossRef
  5. Sinha B, Annachhatre AP. 2006. Partial nitrification - operational parameters and microorganisms involved. Rev. Environ. Sci. Biotechnol. 6: 285-313.
    CrossRef
  6. Third KA, Sliekers AO, Kuenen JG, Jetten MS. 2001. The CANON system (Completely Autotrophic Nitrogen-removal Over Nitrite) under ammonium limitation: interaction and competition between three groups of bacteria. Syst. Appl. Microbiol. 24: 588-596.
    Pubmed CrossRef
  7. Wang L, Zheng P, Chen TT, Chen JW, Xing YJ, Ji QX, et al. 2012. Performance of autotrophic nitrogen removal in the granular sludge bed reactor. Bioresour. Technol. 123: 78-85.
    Pubmed CrossRef
  8. Varas R, Guzmán-Fierro V, Giustinianovich E, Behar J, Fernández K, Roeckel M. 2015. Startup and oxygen concentration effects in a continuous granular mixed flow autotrophic nitrogen removal reactor. Bioresour. Technol. 190: 345-351.
    Pubmed CrossRef
  9. Vázquez-Padín J, Mosquera-Corral A, Campos JL, Méndez R, Revsbech NP. 2010. Microbial community distribution and activity dynamics of granular biomass in a CANON reactor. Water Res. 44: 4359-4370.
    Pubmed CrossRef
  10. Vlaeminck SE, Terada A, Smets BF, De Clippeleir H, Schaubroeck T, Bolca S, et al. 2010. Aggregate size and architecture determine microbial activity balance for one-stage partial nitritation and anammox. Appl. Environ. Microbiol. 76: 900-909.
    Pubmed KoreaMed CrossRef
  11. Volcke EI, Picioreanu C, De Baets B, van Loosdrecht MCM. 2012. The granule size distribution in an anammox-based granular sludge reactor affects the conversion - implications for modeling. Biotechnol. Bioeng. 109: 1629-1636.
    Pubmed CrossRef
  12. Lotti T, Kleerebezem R, Hu Z, Kartal B, Jetten MS, van Loosdrecht MCM. 2014. Simultaneous partial nitritation and anammox at low temperature with granular sludge. Water Res. 66: 111-121.
    Pubmed CrossRef
  13. Guo JH, P eng YZ, F an L , Zhang L, N i BJ, Kartal B , et al. 2016. Metagenomic analysis of anammox communities in three different microbial aggregates. Environ. Microbiol. 18: 2979-2993.
    Pubmed CrossRef
  14. Pérez J, Lotti T, Kleerebezem R, Picioreanu C, van Loosdrecht MCM. 2014. Outcompeting nitrite-oxidizing bacteria in single-stage nitrogen removal in sewage treatment plants:a model-based study. Water Res. 66: 208-218.
    Pubmed CrossRef
  15. Wang L, Zheng P, Xing YJ, Li W, Yang J, Abbas G, et al. 2014. Effect of particle size on the performance of autotrophic nitrogen removal in the granular sludge bed reactor and microbiological mechanisms. Bioresour. Technol. 157: 240-246.
    Pubmed CrossRef
  16. Qian FY, Wang JF, Shen YL, Wang Y, Wang SY, Chen X. 2017. Achieving high performance completely autotrophic nitrogen removal in a continuous granular sludge reactor. Biochem. Eng. J. 118: 97-104.
    CrossRef
  17. APHA. 1998. Standard Methods for Examination of Water and Wastewater, 20th Ed. American Public Health Association, Washington, DC, USA.
  18. Adav SS, Lee DJ. 2008. Extraction of extracellular polymeric substances from aerobic granule with compact interior structure. J. Hazard. Mater. 154: 1120-1126.
    Pubmed CrossRef
  19. Bassin JP, Kleerebezem R, Dezotti M, van Loosdrecht MCM. 2012. Measuring biomass specific ammonium, nitrite and phosphate uptake rates in aerobic granular sludge. Chemosphere 89: 1161-1168.
    Pubmed CrossRef
  20. Wang JF , Qian F Y, L iu XP, L iu W R, W ang SY, Shen Y L. 2016. Cultivation and characteristics of partial nitrification granular sludge in a sequencing batch reactor inoculated with heterotrophic granules. Appl. Microbiol. Biotechnol. 100:9381-9391.
    Pubmed CrossRef
  21. Ohene-Adjei S, Teather RM, Ivan M, Forster RJ. 2007. Postinoculation protozoan establishment and association patterns of methanogenic archaea in the ovine rumen. Appl. Environ. Microbiol. 73: 4609-4618.
    Pubmed KoreaMed CrossRef
  22. Stahl DA, de la Torre JR. 2012. Physiology and diversity of ammonia-oxidizing archaea. Annu. Rev. Microbiol. 66: 83-101.
    Pubmed CrossRef
  23. Vlaeminck SE, Terada A, Smets BF, van der Linden D, Boon N, Verstraete W, et al. 2009. Nitrogen removal from digested black water by one-stage partial nitritation and anammox. Environ. Sci. Technol. 43: 5035-5041.
    Pubmed CrossRef
  24. Lv YT, Wang L, Sun T, Wang XD, Yang YZ, Wang ZY. 2010. Autotrophic nitrogen removal discovered in suspended nitritation system. Chemosphere 79: 180-185.
    Pubmed CrossRef
  25. Winkler MK, Kleerebezem R, Kuenen JG, Yang J, van Loosdrecht MCM. 2011. Segregation of biomass in cyclic anaerobic/aerobic granular sludge allows the enrichment of anaerobic ammonium oxidizing bacteria at low temperatures. Environ. Sci. Technol. 45: 7330-7337.
    Pubmed CrossRef
  26. Verawaty M, Pijuan M, Yuan Z, Bond PL. 2012. Determining the mechanisms for aerobic granulation from mixed seed of floccular and crushed granules in activated sludge wastewater treatment. Water Res. 46: 761-771.
    Pubmed CrossRef
  27. Li XJ, Sun S, Badgley BD, Sung S, Zhang H, He Z. 2016. Nitrogen removal by granular nitritation-anammox in an upflow membrane-aerated biofilm reactor. Water Res. 94: 23-31.
    Pubmed CrossRef
  28. Li W, Zheng P, Ji JY, Zhang M, Guo J, Zhang JQ, et al. 2014. Floatation of granular sludge and its mechanism: a key approach for high-rate denitrifying reactor. Bioresour. Technol. 152: 414-419.
    Pubmed CrossRef
  29. Hubaux N, Wells G, Morgenroth E. 2015. Impact of coexistence of flocs and biofilm on performance of combined nitritationanammox granular sludge reactors. Water Res. 68: 127-139.
    Pubmed CrossRef
  30. Cho S, Fujii N, Lee T, Okabe S. 2011. Development of a simultaneous partial nitrification and anaerobic ammonia oxidation process in a single reactor. Bioresour. Technol. 102:652-659.
    Pubmed CrossRef
  31. Bartrolí A, Pérez J, Carrera J. 2010. Applying ratio control in a continuous granular reactor to achieve full nitritation under stable operating conditions. Environ. Sci. Technol. 44: 8930-8935.
    Pubmed CrossRef
  32. Tang CJ, Zheng P, Wang CH, Mahmood Q, Zhang JQ, Chen XG, et al. 2011. Performance of high-loaded ANAMMOX UASB reactors containing granular sludge. Water Res. 45: 135-144.
    Pubmed CrossRef
  33. Oshiki M, Satoh H, Okabe S. 2016. Ecology and physiology of anaerobic ammonium oxidizing bacteria. Environ. Microbiol. 18: 2784-2796.
    Pubmed CrossRef
  34. Ma B, Bao P, Wei Y, Zhu GB, Yuan ZG, Peng YZ. 2015. Suppressing nitrite-oxidizing bacteria growth to achieve nitrogen removal from domestic wastewater via anammox using intermittent aeration with low dissolved oxygen. Sci. Rep. 5: 13048-13057.
    Pubmed KoreaMed CrossRef
  35. Wett B, Omari A, Podmirseg SM, Han M, Akinayo O, Gómez Brandón M, et al. 2013. Going for mainstream deammonification from bench to full scale for maximized resource efficiency. Water Sci. Technol. 68: 283-289.
    Pubmed CrossRef
  36. Regmi P, Mark WM, Holgate B, Bunce R, Park H, Chandran K, et al. 2014. Control of aeration, aerobic SRT and COD input for mainstream nitritation/denitritation. Water Res. 57: 162-171.
    Pubmed CrossRef
  37. Nowka B, Daims H, Spieck E. 2015. Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Appl. Environ. Microbiol. 81: 745-753.
    Pubmed KoreaMed CrossRef
  38. Zhang L, Liu MM, Zhang SJ, Yang YD, Peng YZ. 2015. Integrated fixed-biofilm activated sludge reactor as a powerful tool to enrich anammox biofilm and granular sludge. Chemosphere 140: 114-118.
    Pubmed CrossRef
  39. Han M, Vlaeminck SE, Al-Omari A, Wett B, Bott C, Murthy S, et al. 2016. Uncoupling the solids retention times of flocs and granules in mainstream deammonification: a screen as effective out-selection tool for nitrite oxidizing bacteria. Bioresour. Technol. 221: 195-204.
    Pubmed CrossRef