New concepts of microbial treatment processes for the nitrogen removal in wastewater

FEMS Microbiology Reviews

Volumn 27, Issue 4, 2003, Pages 481-492

  Schmidt, Ingo ^a   Sliekers, Olav ^b   Schmid, Markus ^b   Bock, Eberhard ^c   Fuerst, John ^d   Kuenen, J Gijs ^b   Jetten, Mike S M ^a   Strous, Marc ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^c UNIVERSITY OF HAMBURG   (Germany)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Aerobic and anaerobic ammonia oxidation; Anammox; Canon; Nitrification; Nitrogen removal; NOx cycle; SHARON; Wastewater treatment

Indexed keywords

AMMONIA; NITRITE; NITROGEN; OXIDIZING AGENT;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; ATMOSPHERE; BACTERIAL STRAIN; COST EFFECTIVENESS ANALYSIS; DENITRIFICATION; ECOLOGICAL NICHE; MICROBIAL ACTIVITY; MICROBIAL CONTAMINATION; MICROBIOLOGICAL EXAMINATION; NITRIFICATION; NITROGEN CYCLE; NONHUMAN; PHYLOGENY; REVIEW; WASTE WATER MANAGEMENT;

EID: 0141671803     PISSN: 01686445     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-6445(03)00039-1     Document Type: Review

References (101)

1. Daims H., Nielsen P.H., Nielsen J.L., Juretschko S., Wagner M. Novel Nitrospira-like bacteria as dominant nitrite-oxidizers in biofilms from wastewater treatment plants: diversity and in situ physiology. Water Sci. Technol. 41:2000;85-90.
2. Juretschko S., Timmermann G., Schmid M., Schleifer K.H., Pommerening-Roser A., Koops H.P., Wagner M. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge - Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl. Environ. Microbiol. 64:1998;3042-3051.
3. Purkhold U., Pommerening-Roser A., Juretschko S., Schmid M.C., Koops H.P., Wagner M. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl. Environ. Microbiol. 66:2000;5368-5382.
4. Schramm A., De Beer D., Wagner M., Amann R.I. Identification and activities in situ of Nitrosospira and Nitrospira spp. as dominant populations in a nitrifying fluidized bed reactor. Appl. Environ. Microbiol. 64:1998;3480-3485.
5. Helmer C., Kunst S., Juretschko S., Schmid M.C., Schleifer K.H., Wagner M. Nitrogen loss in a nitrifying biofilm system. Water Sci. Technol. 39:1999;13-21.
6. Schmid M., Twachtmann U., Klein M., Strous M., Juretschko S., Jetten M., Metzger J.W., Schleifer K.H., Wagner M. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst. Appl. Microbiol. 23:2000;93-106.
7. Egli K., Fanger U., Alvarez P.J.J., Siegrist H., Van der Meer J.R., Zehnder A.J.B. Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch. Microbiol. 175:2001;198-207.
8. Gieseke A., Purkhold U., Wagner M., Amann R., Schramm A. Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Appl. Environ. Microbiol. 67:2001;1351-1362.
9. Schmid M., Schmitz-Esser S., Jetten M., Wagner M. 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium-oxidizing bacteria: implications for phylogeny and in situ detection. Environ. Microbiol. 3:2001;450-459.
10. Bateman A. The structure of a domain common to Archaebacteria and the homocystinuria disease protein. Trends Biochem. Sci. 22:1997;12-13.
11. Steinert K., Wagner V., Kroth-Pancic P.G., Bickel-Sandkotter S. Characterization and subunit structure of the ATP synthase of the halophilic archaeon Haloferax volcanii and organization of the ATP synthase genes. J. Biol. Chem. 272:1997;6261-6269.
12. De Bie M.J.M., Speksnijder A.G.C.L., Kowalchuk G.A., Schuurman T., Zwart G., Stephen J.R., Diekmann O.E., Laanbroek H.J. Shifts in the dominant populations of ammonia-oxidizing β-subclass Proteobacteria along the eutrophic Schelde estuary. Aquat. Microb. Ecol. 23:2001;225-236.
13. Kowalchuk G.A., Bodelier P.L.E., Heilig G.H.J., Stephen J.R., Laanbroek H.J. Community analysis of ammonia-oxidising bacteria, in relation to oxygen availability in soils and root-oxygenated sediments, using PCR, DGGE and oligonucleotide probe hybridisation. FEMS Microbiol. Ecol. 27:1998;339-350.
14. Speksnijder A.G.C.L., Kowalchuk G.A., Roest K., Laanbroek H.J. Recovery of a Nitrosomonas-like 16S rDNA sequence group from freshwater habitats. Syst. Appl. Microbiol. 21:1998;321-330.
15. Kowalchuk G.A., Stienstra A.W., Heilig G.H.J., Stephen J.R., Woldendorp J.W. Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ. Microbiol. 2:2000;99-110.
16. Nold S.C., Zhou J.Z., Devol A.H., Tiedje J.M. Pacific northwest marine sediments contain ammonia-oxidizing bacteria in the beta subdivision of the Proteobacteria. Appl. Environ. Microbiol. 66:2000;4532-4535.
17. Phillips C.J., Harris D., Dollhopf S.L., Gross K.L., Prosser J.I., Paul E.A. Effects of agronomic treatments on structure and function of ammonia-oxidizing communities. Appl. Environ. Microbiol. 66:2000;5410-5418.
18. Logemann S., Schantl J., Bijvank S., Van Loosdrecht M.C.M., Kuenen J.G., Jetten M. Molecular microbial diversity in a nitrifying reactor system without sludge retention. FEMS Microbiol. Ecol. 27:1998;239-249.
19. Prosser, J.I. (1989) Autotrophic nitrification in bacteria. In: Advances in Microbial Physiology, Vol. 30 (Rose, A.H. and Tempest, D.W., Eds.), pp. 125-181. Academic Press, London.
20. Ehrich S., Behrens D., Lebedeva E., Ludwig W., Bock E. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp nov and its phylogenetic relationship. Arch. Microbiol. 164:1995;16-23.
21. Bock, E., Koops, H.-P., Harms, H. and Ahlers, B. (1991) The biochemistry of nitrifying organisms. In: Variations of Autotrophic Life (Shively, J.M., Ed.), pp. 171-200. Academic Press, London.
22. Watson, S.W., Bock, E., Harms, H., Koops, H.-P. and Hooper, A.B. (1989) Nitrifying bacteria. In: Bergey's Manual of Systematic Bacteriology (Stanley, J.T., Bryant, M.P., Pfennig, N. and Holt, J.G., Eds.), pp. 1808-1834. Williams and Wilkens, Baltimore, MD.
23. Strous M., Fuerst J.A., Kramer E.H.M., Logemann S., Muyzer G., Van de Pas-Schoonen K.T., Webb R., Kuenen J.G., Jetten M.S.M. Missing lithotroph identified as new planctomycete. Nature. 400:1999;446-449.
24. Jetten M.S.M., Wagner M., Fuerst J., Van Loosdrecht M.C.M., Kuenen G., Strous M. Microbiology and application of the anaerobic ammonium oxidation ('anammox') process. Curr. Opin. Biotechnol. 12:2001;283-288.
25. Hippen A., Helmer C., Kunst S., Rosenwinkel K.H., Seyfried C.F. Six years' practical experience with aerobic/anoxic deammonification in biofilm systems. Water Sci. Technol. 44:2001;39-48.
26. Koops H.P., Pommerening-Roser A. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 37:2001;1-9.
27. Rees M., Nason A. Incorporation of atmospheric oxygen into nitrite formed during ammonia oxidation by Nitrosomonas europaea. Biochim. Biophys. Acta. 113:1966;398-401.
28. Schmidt I., Bock E. Anaerobic ammonia oxidation with nitrogen dioxide by Nitrosomonas eutropha. Arch. Microbiol. 167:1997;106-111.
29. 15N-NMR evidence. FEBS Lett. 164:1983;236-240.
30. Dua R.D., Bhandari B., Nicholas D.J.D. Stable isotope studies on the oxidation of ammonia to hydroxylamine by Nitrosomonas europaea. FEBS Lett. 106:1979;401-404.
31. Hyman M.R., Wood P.M. Suicidal inactivation and labeling of ammonia monooxygenase by acetylene. Biochem. J. 227:1985;719-725.
32. Hyman M.R., Arp D.J. An electrophoretic study of the thermal-dependent and reductant-dependent aggregation of the 28 kDa component of ammonia monooxygenase from Nitrosomonas europaea. Electrophoresis. 14:1993;619-627.
33. Schmidt I., Bock E. Anaerobic ammonia oxidation by cell free extracts of Nitrosomonas eutropha. Antonie van Leeuwenhoek. 73:1998;271-278.
34. Arciero D.M., Hooper A.B. Hydroxylamine oxidoreductase from Nitrosomonas europaea is a multimer of an octa-heme subunit. J. Biol. Chem. 268:1993;14645-14654.
35. Bergmann D.J., Arciero D.A., Hooper A.B. Organization of the hao gene cluster of Nitrosomonas europaea: genes for two tetraheme c cytochromes. J. Bacteriol. 176:1994;3148-3153.
36. Sayavedra-Soto L.A., Hommes N.G., Arp D.J. Characterization of the gene encoding hydroxylamine oxidoreductase in Nitrosomonas europaea. J. Bacteriol. 176:1994;504-510.
37. Wood, P.M. (1986) Nitrification as a bacterial energy source. In: Nitrification (Prosser, J.L., Ed.), pp. 63-78. IRL Press, Oxford.
38. Hyman M.R., Wood P.M. Methane oxidation by Nitrosomonas europaea. Biochem. J. 212:1983;31-37.
39. Hyman M.R., Sansome-Smith A.W., Shears J.H., Wood R.M. A kinetic study of benzene oxidation to phenol by whole cells of Nitrosomonas europaea and evidence for further oxidation to hydroquinone. Arch. Microbiol. 43:1985;302-306.
40. Hynes R.K., Knowles R. Inhibition by acetylene of ammonia oxidation in Nitrosomonas europaea. FEMS Microbiol. Lett. 4:1978;319-321.
41. 2 as oxidant is not inhibited by acetylene. Microbiology. 147:2001;2247-2253.
42. 2 or NO. Arch. Microbiol. 169:1998;282-286.
43. 2O production by Nitrosomonas europaea: an examination of nitrifier denitrification. Appl. Environ. Microbiol. 49:1985;1134-1141.
44. Poth M. Dinitrogen production from nitrite by a Nitrosomonas isolate. Appl. Environ. Microbiol. 52:1986;957-959.
45. 2 as a regulator for ammonia oxidation of Nitrosomonas eutropha. Antonie van Leeuwenhoek. 79:2001;311-318.
46. Mancinelli R.L., McKay C.P. Effects of nitric oxide and nitrogen dioxide on bacterial growth. Appl. Environ. Microbiol. 46:1983;198-202.
47. Both G.J., Gerards S., Laanbroek H.J. Kinetics of nitrite oxidation in two Nitrobacter species grown in nitrite-limited chemostats. Arch. Microbiol. 157:1992;436-441.
48. Hellinga C., Schellen A.A.J.C., Mulder J.W., Van Loosdrecht M.C.M., Heijnen J.J. The SHARON process: an innovative method for nitrogen removal from ammonium-rich waste water. Water Sci. Technol. 37:1998;135-142.
49. Sundermeyer H., Bock E. Energy metabolism of autotrophically and heterotrophically grown cells of Nitrobacter winogradskyi. Arch. Microbiol. 130:1981;250-254.
50. 1 from Nitrobacter agilis and characterization of nitrite oxidation system of the bacterium. Arch. Microbiol. 135:1983;265-271.
51. Aleem M.I.H., Hoch G.E., Varner J.E. Water as the source of oxidant and reductant in bacterial chemosynthesis. Proc. Natl. Acad. Sci. USA. 54:1965;869-873.
52. Hollocher T.C., Kumar S., Nicholas D.J.D. Respiration-dependent proton translocation in Nitrosomonas europaea and its apparent absence in Nitrobacter agilis during inorganic oxidations. J. Bacteriol. 149:1982;1013-1020.
53. Sone N., Yanagita Y., Hon-Nami K., Fukumori Y., Yamanaka T. Proton-pump activity of Nitrobacter agilis and Thermus thermophilus cytochrome c oxidases. FEBS Lett. 155:1983;150-153.
54. Bock E., Düvel D., Peters K.-R. Characterization of a phage-like particle from cells of Nitrobacter. I. Host-particle correlation and particle isolation. Arch. Microbiol. 97:1974;115-127.
55. Steinmüller W., Bock E. Growth of Nitrobacter in the presence of organic matter. I. Mixotrophic growth. Arch. Microbiol. 108:1976;299-304.
56. Watson S.W., Bock E., Valois F.W., Waterbury J.B., Schlosser U. Nitrospira marina gen. nov. sp. nov. a chemolithotrophic nitrite oxidizing bacterium. Arch. Microbiol. 144:1986;1-7.
57. Bock E. Growth of Nitrobacter in the presence of organic matter. II. Chemoorganic growth of Nitrobacter agilis. Arch. Microbiol. 108:1976;305-312.
58. Steinmüller W., Bock E. Enzymatic studies on autotrophically, mixotrophically and heterotrophically grown Nitrobacter agilis with special references to nitrite oxidase. Arch. Microbiol. 115:1977;51-54.
59. Bock E., Wilderer P.A., Freitag A. Growth of Nitrobacter in the absence of dissolved oxygen. Water Res. 22:1988;245-250.
60. Sundermeyer-Klinger H., Meyer W., Warninghoff B., Bock E. Membrane-bound nitrite oxidoreductase of Nitrobacter: evidence for a nitrate reductase system. Arch. Microbiol. 140:1984;153-158.
61. Hanaki K., Wantawin C., Ogaki S. Nitrification at low levels of dissolved oxygen with and without organic loading in a suspended-growth reactor. Water Res. 24:1990;297-302.
62. Eigner U., Bock E. Synthesis and breakdown of polyphosphate fraction in cells of Nitrobacter winogradskyi. Arch. Mikrobiol. 81:1972;367-378.
63. Strous M., Heijnen J.J., Kuenen J.G., Jetten M.S.M. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Microbiol. Biotechnol. 50:1998;589-596.
64. Strous M., Kuenen J.G., Jetten M.S.M. Key physiology of anaerobic ammonium oxidation. Appl. Environ. Microbiol. 65:1999;3248-3250.
65. Strous M., Van Gerven E., Kuenen J.G., Jetten M. Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (Anammox) sludge. Appl. Environ. Microbiol. 63:1997;2446-2448.
66. Van de Graaf A.A., De Bruijn P., Robertson L.A., Jetten M.S.M., Kuenen J.G. Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology UK. 142:1996;2187-2196.
67. Van de Graaf A.A., De Bruijn P., Robertson L.A., Jetten M.S.M., Kuenen J.G. Metabolic pathway of anaerobic ammonium oxidation on the basis of N-15 studies in a fluidized bed reactor. Microbiology UK. 143:1997;2415-2421.
68. Schalk J., De Vries S., Kuenen J.G., Jetten M.S.M. Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry. 39:2000;5405-5412.
69. Lindsay M.R., Webb R.I., Strous M., Jetten M.S., Butler M.K., Forde R.J., Fuerst J.A. Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch. Microbiol. 175:2001;413-429.
70. Sinninghe Damsté J.S., Strous M., Rijpstra W.I.C., Hopmans E.C., Geenevasen J.A.J., Van Duin A.C.T., Van Niftrik L.A., Jetten M.S.M. Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature. 419:2002;708-712.
71. Van Niel E.W.J., Arts P.A.M., Wesselink B.J., Robertson L.A., Kuenen J.G. Competition between heterotrophic and autotrophic nitrifiers for ammonia in chemostat cultures. FEMS Microbiol. Ecol. 102:1993;109-118.
72. Ralt D., Gomez R.F., Tannerbaum S.R. Conversion of acetohydroxamate and hydroxylamine to nitrite by intestinal microorganisms. Eur. J. Appl. Microbiol. Biotechnol. 12:1981;226-230.
73. Castignetti D., Hollocher T.C. Heterotrophic nitrification among denitrifiers. Appl. Environ. Microbiol. 47:1984;620-623.
74. Wood, P.M. (1988) Monooxygenase and free radical mechanism for biological ammonia oxidation. In: The Nitrogen and Sulfur Cycles (Cole, J.A., Ed.), pp. 217-243. Cambridge University Press, Cambridge.
75. Spiller H., Dietsch E., Kessler E. Intracellular appearance of nitrite and nitrate in nitrogen-starved cells of Ankistrodesmus braunii. Planta. 129:1976;175-181.
76. Stams A.J.M., Flameling E.M., Marnette E.C.L. The importance of autotrophic versus heterotrophic oxidation of atmospheric ammonium in forest ecosystems with acid soil. FEMS Microbiol. Ecol. 74:1990;337-344.
77. Robertson L.A., Kuenen J.G. Combined heterotrophic nitrification and aerobic denitrification in Thiosphaera pantotropha and other bacteria. Antonie van Leeuwenhoek. 57:1990;139-152.
78. Robertson L.A., Kuenen J.G. Heterotrophic nitrification in Thiosphaera pantotropha: oxygen uptake and enzyme studies. J. Gen. Microbiol. 134:1988;857-863.
79. Killham, K. (1986) Heterotrophic nitrification. In: Nitrification (Prosser, J.I., Ed.), pp. 117-126. IRL Press, Oxford.
80. Shoun H., Tanimoto T. Denitrification by the fungus Fusarium oxysporum and involvement of cytochrome P-450 in the respiratory nitrite reduction. J. Biol. Chem. 25:1991;1527-1536.
81. Zumft W.G. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61:1997;533-616.
82. Focht D.D., Chang A.C. Nitrification and denitrification process related to wastewater treatment. Adv. Appl. Microbiol. 19:1975;153-186.
83. Zumft, W.G., Viebrock, A. and Körner, H. (1988) Biochemical and physiological aspects of denitrification. In: The Nitrogen and Sulfur Cycles (Cole, J.A. and Ferguson, S.J., Eds.), pp. 245-279. Cambridge University Press, Cambridge.
84. Zumft W.G., Körner H. Enzyme diversity and mosaic gene organization in denitrification. Antonie van Leeuwenhoek. 71:1997;43-58.
85. Zumft, W.G. (1992) The denitrifying prokaryotes. In: The Prokaryotes, 2nd edn. (Balows, A., Trüper, H.G., Dworkin, M., Harder, W. and Schleifer, K.-H., Eds.), pp. 554-582. Springer, New York.
86. Körner H., Zumft W.G. Expression of denitrification enzymes in response to the dissolved oxygen level and respiratory substrate in continuous culture of Pseudomonas stuzeri. Appl. Environ. Microbiol. 55:1989;1670-1676.
87. Hellinga C., Van Loosdrecht M.C.M., Heijnen J.J. Model based design of a novel process for nitrogen removal from concentrated flows. Math. Comp. Model Dyn. 5:1999;351-371.
88. Mulder J.W., Van Loosdrecht M.C.M., Hellinga C., Van Kempen R. Full-scale application of the SHARON process for treatment of rejection water of digested sludge dewatering. Water Sci. Technol. 43:2001;127-134.
89. Strous M., Van Gerven E., Ping Z., Kuenen J.G., Jetten M.S.M. Ammonium removal from concentrated waste streams with the Anaerobic Ammonium Oxidation (Anammox) process in different reactor configurations. Water Res. 31:1997;1955-1962.
90. Mulder, A. (1992) Anoxic ammonia oxidation. U.S. Patent documents 427849.
91. Van Loosdrecht, M.C.M. and Jetten, M.S.M. (1997) Method for treating ammonia-comprising wastewater. PCT/NL97/00482.
92. Van Dongen U., Jetten M.S.M., Van Loosdrecht M.C.M. The SHARON((R))-Anammox((R)) process for treatment of ammonium rich wastewater. Water Sci. Technol. 44:2001;153-160.
93. Koch G., Egli K., Van der Meer J.R., Siegrist H. Mathematical modeling of autotrophic denitrification in a nitrifying biofilm of a rotating biological contactor. Water Sci. Technol. 41:2000;191-198.
94. Third K.A., Sliekers A.O., Kuenen J.G., Jetten M.M. The CANON System (Completely Autotrophic Nitrogen-removal Over Nitrite) under ammonium limitation: Interaction and competition between three groups of bacteria. Syst. Appl. Microbiol. 24:2002;588-596.
95. Siegrist H., Reithaar S., Koch G., Lais P. Nitrogen loss in a nitrifying rotating contactor treating ammonium-rich wastewater without organic carbon. Water Sci. Technol. 38:1998;241-248.
96. Helmer C., Tromm C., Hippen A., Rosenwinkel K.H., Seyfried C.F., Kunst S. Single stage biological nitrogen removal by nitritation and anaerobic ammonium oxidation in biofilm systems. Water Sci. Technol. 43:2001;311-320.
97. Hippen A., Rosenwinkel K.H., Baumgarten G., Seyfried C.F. Aerobic deammonification - a new experience in the treatment of wastewaters. Water Sci. Technol. 35:1997;111-120.
98. Bock, E., Schmidt, I., Stüven, R. and Zart, D. (1996) Verfahren zur biologischen Umsetzung von in Wasser gelöstem Ammonium unter Verwendung ammoniak-oxidierender Bakterien. Az.: DE 196 17 331.0-41.
99. Schmidt I., Zart D., Stüven R., Bock E. Ein neues Verfahren zur Entfernung von Ammonium-Stickstoff aus Abwasser. Chem. Ing. Tech. 73:2001;879-882.
100. Kuai L., Verstraete W. Ammonium removal by the oxygen-limited autotrophic nitrification-denitrification system. Appl. Environ. Microbiol. 64:1998;4500-4506.
101. Schmidt I., Hermelink C., Van de Pas-Schoonen K., Strous M., op den Camp H.J., Kuenen J.G., Jetten M.S.M. Anaerobic ammonia oxidation in the presence of nitrogen oxides (NOx) by two different lithotrophs. Appl. Environ. Microbiol. 68:2002;5351-5357.