Aerobic denitrification: A review of important advances of the last 30 years

Abstract

Understanding aerobic denitrification has become an important focus of environmental microbiology. Aerobic denitrification can be performed by various genera of microorganisms and describes the use of nitrate (NO -3 ) as oxidizing agents under an aerobic atmosphere. Isolation of aerobic denitrifiers, enzymes involved in aerobic denitrifiers, phylogenetic distribution of aerobic denitrifiers, factors affecting the performance of aerobic denitrifiers, attempts of applications and possible future trends are depicted. The periplasmic nitrate reductase is vital for aerobic denitrifiers and NapA gene may be the proof of aerobic denitrification. Phylogenetic analysis revealed that aerobic denitrifiers mainly belong to α-, β- and γ-Proteobacteria. Aerobic denitrifiers tend to work efficiently at 25 ~ 37°C and pH 7 ~ 8, when dissolved oxygen concentration is 3 ~ 5 mg/L and C/N load ratio is 5 ~ 10. In addition, recent progresses and applications on aerobic denitrifiers are described, including single aerobic reactors, sequencing batch reactor and biofilm reactors. The review attempts to shed light on the fundamental understanding in aerobic denitrification.

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References

  1. 1.

    Seifi, M. and M. H. Fazaelipoor (2012) Modeling simultaneous nitrification and denitrification (SND) in a fluidized bed biofilm reactor. Appl. Math. Model. 36: 5603–5613.

    Article  Google Scholar 

  2. 2.

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

    CAS  Article  Google Scholar 

  3. 3.

    Padhi, S. K., S. Tripathy, R. Sen, A. S. Mahapatra, S. Mohanty, and N. K. Maiti (2013) Characterisation of heterotrophic nitrifying and aerobic denitrifying Klebsiella pneumoniae CF-S9 strain for bioremediation of wastewater. Int. Biodeter. Biodegr. 78: 67–73.

    CAS  Article  Google Scholar 

  4. 4.

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

    CAS  Article  Google Scholar 

  5. 5.

    Robertson, L. A. and J. G. Kuenen (1984) Aerobic denitrification—old wine in new bottles? Antonie Van Leeuwenhoek 50: 525–544.

    CAS  Article  Google Scholar 

  6. 6.

    Ludwig, W., G. Mittenhuber, and C. G. Friedrich (1993) Transfer of Thiosphaera pantotropha to Paracoccus denitrificans. Int. J. Syst. Bacteriol. 43: 363–367.

    CAS  Article  Google Scholar 

  7. 7.

    Robertson, L. A., E. W. van Niel, R. A. Torremans, and J. G. Kuenen (1988) Simultaneous nitrification and denitrification in aerobic chemostat cultures of Thiosphaera pantotropha. Appl. Environ. Microbiol. 54: 2812–2818.

    CAS  Google Scholar 

  8. 8.

    Lukow, T. and H. Diekmann (1997) Aerobic denitrification by a newly isolated heterotrophic bacterium strain TL1. Biotechnol. Lett. 19: 1157–1159.

    CAS  Article  Google Scholar 

  9. 9.

    Kong, Q. X., X. W. Wang, M. Jin, Z. Q. Shen, and J. W. Li (2006) Development and application of a novel and effective screening method for aerobic denitrifying bacteria. FEMS Microbiol. Lett. 260: 150–155.

    CAS  Article  Google Scholar 

  10. 10.

    Chen, Q. and J. Ni (2011) Heterotrophic nitrification-aerobic denitrification by novel isolated bacteria. J. Ind. Microbiol. Biotechnol. 38: 1305–1310.

    CAS  Article  Google Scholar 

  11. 11.

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

    CAS  Article  Google Scholar 

  12. 12.

    Ji, B., H. Wang, and K. Yang (2014) Tolerance of an aerobic denitrifier (Pseudomonas stutzeri) to high O2 concentrations. Biotechnol. Lett. 36: 719–722.

    CAS  Article  Google Scholar 

  13. 13.

    Patureau, D., J. Davison, N. Bernet, and R. Moletta (1994) Denitrification under various aeration conditions in Comamonas sp., strain SGLY2. FEMS Microbiol. Ecol. 14: 71–78.

    CAS  Article  Google Scholar 

  14. 14.

    Kim, J. K., K. J. Park, K. S. Cho, S. Nam, T. Park, and R. Bajpai (2005) Aerobic nitrification-Cdenitrification by heterotrophic Bacillus strains. Bioresour. Technol. 96: 1897–1906.

    CAS  Article  Google Scholar 

  15. 15.

    Su, J. J., B. Y. Liu, and C. Y. Liu (2001) Comparison of aerobic denitrification under high oxygen atmosphere by Thiosphaera pantotropha ATCC 35512 and Pseudomonas stutzeri SU2 newly isolated from the activated sludge of a piggery wastewater treatment system. J. Appl. Microbiol. 90: 457–462.

    CAS  Article  Google Scholar 

  16. 16.

    Chen, P., J. Li, Q. X. Li, Y. Wang, S. Li, T. Ren, and L. Wang (2012) Simultaneous heterotrophic nitrification and aerobic denitrification by bacterium Rhodococcus sp. CPZ24. Bioresour. Technol. 116: 266–270.

    CAS  Article  Google Scholar 

  17. 17.

    Huang, H. K. and S. K. Tseng (2001) Nitrate reduction by Citrobacter diversus under aerobic environment. Appl. Microbiol. Biot. 55: 90–94.

    CAS  Article  Google Scholar 

  18. 18.

    Okada, N. N. N. K. (2005) Characterization of the aerobic denitrification in Mesorhizobium sp. strain NH-14 in comparison with that in related Rhizobia. Microbes Environ. 20: 208–215.

    Google Scholar 

  19. 19.

    Nakano, M., T. Inagaki, S. Okunishi, R. Tanaka, and H. Maeda (2010) Effect of salinity on denitrification under limited single carbon source by Marinobacter sp. isolated from marine sediment. J. Basic Microbiol. 50: 285–289.

    CAS  Article  Google Scholar 

  20. 20.

    Guo, Y., X. Zhou, Y. Li, K. Li, C. Wang, J. Liu, D. Yan, Y. Liu, D. Yang, and J. Xing (2013) Heterotrophic nitrification and aerobic denitrification by a novel Halomonas campisalis. Biotechnol. Lett. 35: 2045–2049.

    CAS  Article  Google Scholar 

  21. 21.

    Frette, L., B. Gejlsbjerg, and P. Westermann (1997) Aerobic denitrifiers isolated from an alternating activated sludge system. Fems Microbiol. Ecol. 24: 363–370.

    CAS  Article  Google Scholar 

  22. 22.

    Gao, H., F. Schreiber, G. Collins, M. M. Jensen, O. Svitlica, J. E. Kostka, G. Lavik, D. de Beer, H. Y. Zhou, and M. M. Kuypers (2010) Aerobic denitrification in permeable Wadden Sea sediments. ISME J. 4: 417–426.

    CAS  Article  Google Scholar 

  23. 23.

    Takaya, N., M. A. Catalan-Sakairi, Y. Sakaguchi, I. Kato, Z. Zhou, and H. Shoun (2003) Aerobic denitrifying bacteria that produce low levels of nitrous oxide. Appl. Environ. Microbiol. 69: 3152–3157.

    CAS  Article  Google Scholar 

  24. 24.

    Gupta, S. K. and M. Kshirsagar (2000) Quantitative estimation of Thiosphaera pantotropha from aerobic mixed culture. Water Res. 34: 3765–3768.

    CAS  Article  Google Scholar 

  25. 25.

    Kong, Q. X., X. W. Wang, M. Jin, Z. Q. Shen, and J. W. Li (2006) Development and application of a novel and effective screening method for aerobic denitrifying bacteria. Fems Microbiol. Lett. 260: 150–155.

    CAS  Article  Google Scholar 

  26. 26.

    Zhu, L., W. Ding, L. Feng, Y. Kong, J. Xu, and X. Xu (2012) Isolation of aerobic denitrifiers and characterization for their potential application in the bioremediation of oligotrophic ecosystem. Bioresour. Technol. 108: 1–7.

    CAS  Article  Google Scholar 

  27. 27.

    Simon, J. and M. G. Klotz (2013) Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations. Biochimica et Biophysica Acta (BBA) — Bioenergetics 1827: 114–135.

    CAS  Google Scholar 

  28. 28.

    Bell, L. C., D. J. Richardson, and S. J. Ferguson (1990) Periplasmic and membrane-bound respiratory nitrate reductases in Thiosphaera pantotropha: The periplasmic enzyme catalyzes the first step in aerobic denitrification. Febs Lett. 265: 85–87.

    CAS  Article  Google Scholar 

  29. 29.

    Morozkina, E. V. and R. A. Zvyagilskaya (2007) Nitrate reductases: Structure, functions, and effect of stress factors. Biochem. 72: 1151–1160.

    CAS  Google Scholar 

  30. 30.

    Sparacino-Watkins, C., J. F. Stolz, and P. Basu (2014) Nitrate and periplasmic nitrate reductases. Chem. Soc. Rev. 43: 676–706.

    CAS  Article  Google Scholar 

  31. 31.

    Oguz, M. T., K. G. Robinson, A. C. Layton, and G. S. Sayler (2007) Concurrent nitrite oxidation and aerobic denitrification in activated sludge exposed to volatile fatty acids. Biotechnol. Bioeng. 97: 1562–1572.

    CAS  Article  Google Scholar 

  32. 32.

    Feng, W., J. Liu, J. Gu, and B. Mu (2011) Nitrate-reducing community in production water of three oil reservoirs and their responses to different carbon sources revealed by nitrate-reductase encoding gene (napA). Int. Biodeter. Biodegr. 65: 1081–1086.

    CAS  Article  Google Scholar 

  33. 33.

    Chen, J. and M. Strous (2013) Denitrification and aerobic respiration, hybrid electron transport chains and co-evolution. Biochimica et Biophysica Acta (BBA) — Bioenergetics 1827: 136–144.

    CAS  Article  Google Scholar 

  34. 34.

    Nojiri, M., H. Koteishi, T. Nakagami, K. Kobayashi, T. Inoue, K. Yamaguchi, and S. Suzuki (2009) Structural basis of inter-protein electron transfer for nitrite reduction in denitrification. Nature 462: 117–120.

    CAS  Article  Google Scholar 

  35. 35.

    Heylen, K., D. Gevers, B. Vanparys, L. Wittebolle, J. Geets, N. Boon, and P. De Vos (2006) The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environ. Microbiol. 8: 2012–2021.

    CAS  Article  Google Scholar 

  36. 36.

    Ashida, N., S. Ishii, S. Hayano, K. Tago, T. Tsuji, Y. Yoshimura, S. Otsuka, and K. Senoo (2010) Isolation of functional single cells from environments using a micromanipulator: Application to study denitrifying bacteria. Appl. Microbiol. Biotechnol. 85: 1211–1217.

    CAS  Article  Google Scholar 

  37. 37.

    Song, Z. F., J. An, G. H. Fu, and X. L. Yang (2011) Isolation and characterization of an aerobic denitrifying Bacillus sp. YX-6 from shrimp culture ponds. Aquacult. 319: 188–193.

    CAS  Article  Google Scholar 

  38. 38.

    Fujiwara, T. and Y. Fukumori (1996) Cytochrome cb-type nitric oxide reductase with cytochrome c oxidase activity from Paracoccus denitrificans ATCC 35512. J. Bacteriol. 178: 1866–1871.

    CAS  Google Scholar 

  39. 39.

    Kraft, B., M. Strous, and H. E. Tegetmeyer (2011) Microbial nitrate respiration—genes, enzymes and environmental distribution. J. Biotechnol. 155: 104–117.

    CAS  Article  Google Scholar 

  40. 40.

    Orellana, L. H., L. M. Rodriguez-R, S. Higgins, J. C. Chee-Sanford, R. A. Sanford, K. M. Ritalahti, F. E. Loffler, and K. T. Konstantinidis (2014) Detecting nitrous oxide reductase (NosZ) genes in soil metagenomes: method development and implications for the nitrogen cycle. MBio 5: e1114–e1193.

    Article  Google Scholar 

  41. 41.

    Zheng, M., D. He, T. Ma, Q. Chen, S. Liu, M. Ahmad, M. Gui, and J. Ni (2014) Reducing NO and N2O emission during aerobic denitrification by newly isolated Pseudomonas stutzeri PCN-1. Bioresour. Technol. 162: 80–88.

    CAS  Article  Google Scholar 

  42. 42.

    Wan, C., X. Yang, D. Lee, M. Du, F. Wan, and C. Chen (2011) Aerobic denitrification by novel isolated strain using as nitrogen source. Bioresour. Technol. 102: 7244–7248.

    CAS  Article  Google Scholar 

  43. 43.

    Zhou, M., H. Ye, and X. Zhao (2014) Isolation and characterization of a novel heterotrophic nitrifying and aerobic denitrifying bacterium Pseudomonas stutzeri KTB for bioremediation of wastewater. Biotechnol. Bioproc. Eng. 19: 231–238.

    CAS  Article  Google Scholar 

  44. 44.

    Takenaka, S., Q. Zhou, A. Kuntiya, P. Seesuriyachan, S. Murakami, and K. Aoki (2007) Isolation and characterization of thermotolerant bacterium utilizing ammonium and nitrate ions under aerobic conditions. Biotechnol. Lett. 29: 385–390.

    CAS  Article  Google Scholar 

  45. 45.

    Zhang, Q., Y. Liu, G. Ai, L. Miao, H. Zheng, and Z. Liu (2012) The characteristics of a novel heterotrophic nitrification — aerobic denitrification bacterium, Bacillus methylotrophicus strain L7. Bioresour. Technol. 108: 35–44.

    CAS  Article  Google Scholar 

  46. 46.

    Hartsock, A. and J. P. Shapleigh (2011) Physiological roles for two periplasmic nitrate reductases in Rhodobacter sphaeroides 2.4.3 (ATCC 17025). J. Bacteriol. 193: 6483–6489.

    CAS  Article  Google Scholar 

  47. 47.

    Verbaendert, I., N. Boon, P. De Vos, and K. Heylen (2011) Denitrification is a common feature among members of the genus Bacillus. Syst. Appl. Microbiol. 34: 385–391.

    CAS  Article  Google Scholar 

  48. 48.

    Baek, S. H. and J. P. Shapleigh (2005) Expression of nitrite and nitric oxide reductases in free-living and plant-associated Agrobacterium tumefaciens C58 cells. Appl. Environ. Microbiol. 71: 4427–4436.

    CAS  Article  Google Scholar 

  49. 49.

    Bergaust, L., J. Shapleigh, A. Frostegard, and L. Bakken (2008) Transcription and activities of NOx reductases in Agrobacterium tumefaciens: The influence of nitrate, nitrite and oxygen availability. Environ. Microbiol. 10: 3070–3081.

    CAS  Article  Google Scholar 

  50. 50.

    Patureau, D., N. Bernet, J. P. Delgenes, and R. Moletta (2000) Effect of dissolved oxygen and carbon-nitrogen loads on denitrification by an aerobic consortium. Appl. Microbiol. Biotechnol. 54: 535–542.

    CAS  Article  Google Scholar 

  51. 51.

    Wilson, L. P. and E. J. Bouwer (1997) Biodegradation of aromatic compounds under mixed oxygen/denitrifying conditions: a review. J. Ind. Microbiol. Biotechnol. 18: 116–130.

    CAS  Article  Google Scholar 

  52. 52.

    Ka, J. O., J. Urbance, R. W. Ye, T. Y. Ahn, and J. M. Tiedje (1997) Diversity of oxygen and N-oxide regulation of nitrite reductases in denitrifying bacteria. Fems Microbiol. Lett. 156: 55–60.

    CAS  Article  Google Scholar 

  53. 53.

    Chen, Q. and J. Ni (2012) Ammonium removal by Agrobacterium sp. LAD9 capable of heterotrophic nitrification — aerobic denitrification. J. Biosci. Bioeng. 113: 619–623.

    CAS  Google Scholar 

  54. 54.

    Yang, X., S. Wang, D. Zhang, and L. Zhou (2011) Isolation and nitrogen removal characteristics of an aerobic heterotrophic nitrifying-Cdenitrifying bacterium, Bacillus subtilis A1. Bioresour. Technol. 102: 854–862.

    CAS  Article  Google Scholar 

  55. 55.

    Yang, X., S. Wang, and L. Zhou (2012) Effect of carbon source, C/N ratio, nitrate and dissolved oxygen concentration on nitrite and ammonium production from denitrification process by Pseudomonas stutzeri D6. Bioresour. Technol. 104: 65–72.

    CAS  Article  Google Scholar 

  56. 56.

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

    CAS  Article  Google Scholar 

  57. 57.

    Taylor, S. M., Y. He, B. Zhao, and J. Huang (2009) Heterotrophic ammonium removal characteristics of an aerobic heterotrophic nitrifying-denitrifying bacterium, Providencia rettgeri YL. J. Environ. Sci. (China) 21: 1336–1341.

    CAS  Article  Google Scholar 

  58. 58.

    Kim, M., S. Jeong, S. J. Yoon, S. J. Cho, Y. H. Kim, M. J. Kim, E. Y. Ryu, and S. Lee (2008) Aerobic Denitrification of Pseudomonas putida AD-21 at Different C/N Ratios. J. Biosci. Bioeng. 106: 498–502.

    CAS  Article  Google Scholar 

  59. 59.

    Robertson, L. A., R. Cornelisse, P. De Vos, R. Hadioetomo, and J. G. Kuenen (1989) Aerobic denitrification in various heterotrophic nitrifiers. Antonie Van Leeuwenhoek 56: 289–299.

    CAS  Article  Google Scholar 

  60. 60.

    Xie, S. G., X. J. Zhang, and Z. S. Wang (2003) Temperature effect on aerobic denitrification and nitrification. J. Environ. Sci. 15: 669–673.

    CAS  Google Scholar 

  61. 61.

    Saleh-Lakha, S., K. E. Shannon, S. L. Henderson, C. Goyer, J. T. Trevors, B. J. Zebarth, and D. L. Burton (2009) Effect of pH and temperature on denitrification gene expression and activity in Pseudomonas mandelii. Appl. Environ. Microbiol. 75: 3903–3911.

    CAS  Article  Google Scholar 

  62. 62.

    Thomas, K. L., D. Lloyd, and L. Boddy (1994) Effects of oxygen, pH and nitrate concentration on denitrification by Pseudomonas species. Fems Microbiol. Lett. 118: 181–186.

    CAS  Article  Google Scholar 

  63. 63.

    Kshirsagar, M. G. A. B. G.(1995) Aerobic denitrification studies on activated sludge mixed with Thiosphaera pantotropha. Environ. Technol. 16: 35–43.

    CAS  Article  Google Scholar 

  64. 64.

    Patureau, D., N. Bernet, and R. Moletta (1997) Combined nitrification and denitrification in a single aerated reactor using the aerobic denitrifier Commonas sp. strain SGLY2. Water Res. 31: 1363–1370.

    CAS  Article  Google Scholar 

  65. 65.

    Pai, S., N. Chong, and C. Chen (1999) Potential applications of aerobic denitrifying bacteria as bioagents in wastewater treatment. Bioresour. Technol. 68: 179–185.

    CAS  Article  Google Scholar 

  66. 66.

    Patureau, D., E. Helloin, E. Rustrian, T. Bouchez, J. P. Delgenes, and R. Moletta (2001) Combined phosphate and nitrogen removal in a sequencing batch reactor using the aerobic denitrifier, Microvirgula aerodenitrificans. Water Res. 35: 189–197.

    CAS  Article  Google Scholar 

  67. 67.

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

    CAS  Article  Google Scholar 

  68. 68.

    Oguz, M. T., K. G. Robinson, A. C. Layton, and G. S. Sayler (2007) Concurrent nitrite oxidation and aerobic denitrification in activated sludge exposed to volatile fatty acids. Biotechnol. Bioeng. 97: 1562–1572.

    CAS  Article  Google Scholar 

  69. 69.

    Gupta, A. B. and S. K. Gupta (2001) Simultaneous carbon and nitrogen removal from high strength domestic wastewater in an aerobic RBC biofilm. Water Res. 35: 1714–1722.

    CAS  Article  Google Scholar 

  70. 70.

    Ji, B., H. Wang, and K. Yang (2014) Nitrate and COD removal in an upflow biofilter under an aerobic atmosphere. Bioresour. Technol. 158: 156–160.

    CAS  Article  Google Scholar 

  71. 71.

    Jiang, R., S. Huang, A. T. Chow, and J. Yang (2009) Nitric oxide removal from flue gas with a biotrickling filter using Pseudomonas putida. J. Hazard. Mater. 164: 432–441.

    CAS  Article  Google Scholar 

  72. 72.

    Huang, G., H. Fallowfield, H. Guan, and F. Liu (2012) Remediation of nitrate-nitrogen contaminated groundwater by a heterotrophic-autotrophic denitrification approach in an aerobic environment. Water, Air, & Soil Pollution 223: 4029–4038.

    CAS  Article  Google Scholar 

  73. 73.

    Critchley, K., D. L. Rudolph, J. F. Devlin, and P. C. Schillig (2014) Stimulating in situ denitrification in an aerobic, highly permeable municipal drinking water aquifer. J. Contam. Hydrol. 171: 66–80.

    CAS  Article  Google Scholar 

  74. 74.

    Zheng, H., Y. Liu, G. Sun, X. Gao, Q. Zhang, and Z. Liu (2011) Denitrification characteristics of a marine origin psychrophilic aerobic denitrifying bacterium. J. Environ. Sci. 23: 1888–1893.

    CAS  Article  Google Scholar 

  75. 75.

    Schreiber, F., P. Stief, A. Gieseke, I. M. Heisterkamp, W. Verstraete, D. de Beer, and P. Stoodley (2010) Denitrification in human dental plaque. BMC Biol. 8:24.

    Article  Google Scholar 

  76. 76.

    Gunther, S., M. Trutnau, S. Kleinsteuber, G. Hause, T. Bley, I. Roske, H. Harms, and S. Muller (2009) Dynamics of polyphosphate-accumulating bacteria in wastewater treatment plant microbial communities detected via DAPI (4′,6′-diamidino-2-phenylindole) and tetracycline labeling. Appl. Environ. Microbiol. 75: 2111–2121.

    CAS  Article  Google Scholar 

  77. 77.

    Nguyen, H. T., J. L. Nielsen, and P. H. Nielsen (2012) ‘Candidatus Halomonas phosphatis’, a novel polyphosphate-accumulating organism in full-scale enhanced biological phosphorus removal plants. Environ. Microbiol. 14: 2826–2837.

    CAS  Article  Google Scholar 

  78. 78.

    Xu, Y., Z. Xu, Z. Cai, and F. Reverchon (2013) Review of denitrification in tropical and subtropical soils of terrestrial ecosystems. J. Soil. Sediment 13: 699–710.

    CAS  Article  Google Scholar 

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Ji, B., Yang, K., Zhu, L. et al. Aerobic denitrification: A review of important advances of the last 30 years. Biotechnol Bioproc E 20, 643–651 (2015). https://doi.org/10.1007/s12257-015-0009-0

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Keywords

  • aerobic denitrification
  • Pseudomonas stutzeri
  • periplasmic nitrate reductase
  • evolutionary tree
  • Proteobacteria