Molecular and stable isotope methods to detect and measure anaerobic ammonium oxidation (anammox) in aquatic ecosystems

Methods in Enzymology

Volumn 496, Issue , 2011, Pages 63-89

  Song, Bongkeun ^a   Tobias, Craig R ^b  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

16S rRNA; Anammox; hzo1 gene

Indexed keywords

AMMONIA; NITRATE; NITRITE; NITROGEN; RIBOSOME RNA; STABLE ISOTOPE;

AQUATIC ENVIRONMENT; ARTICLE; DENITRIFICATION; OXIDATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEDIMENT;

EID: 79955492406     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386489-5.00003-8     Document Type: Chapter

References (84)

1. T. Amano, I. Yoshinaga, K. Okada, T. Yamagishi, S. Ueda, A. Obuchi, Y. Sako, and Y. Suwa Detection of anammox activity and diversity of anammox bacteria-related 16S rRNA genes in coastal marine sediment in Japan Microbes Environ. 22 2007 232 242
2. N. Byrne, M. Strous, V. Crepeau, B. Kartal, J.L. Birrien, M. Schmid, F. Lesongeur, S. Schlouten, A. Jaeschke, M. Jetten, D. Prieur, and A. Godfroy Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents ISME J. 3 2009 117 123
3. 15 N evidence for anaerobic oxidation (Anammox) Ground Water Monit. Rem. 28 2008 73 82
4. J.C. Cornwell, W.M. Kemp, and T.M. Kana Denitrification in coastal ecosystems: Methods, environmental controls, and ecosystem level controls, a review Aquat. Ecol. 33 1999 41 54 (Pubitemid 30213364)
5. O.R. Dale, C. Tobias, and B. Song Biogeographical distribution of diverse anaerobic ammonium oxidizing (ANAMMOX) bacteria in Cape Fear River Estuary Environ. Microbiol. 11 2009 1194 1207
6. T. Dalsgaard, B. Thamdrup, and D.E. Canfield Mini-review: Anaerobic ammonium oxidation (anammox) in the marine environment Res. Microbiol. 156 2005 457 464 (Pubitemid 40615411)
7. H. Dang, R. Chen, L. Wang, L. Guo, P. Chen, Z. Tang, F. Tian, S. Li, and M.G. Klotz Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China Appl. Environ. Microbiol. 76 2010 7036 7047
8. L.F. Dong, C.J. Smith, S. Papaspyrou, A. Stott, A.M. Osborn, and D.B. Nedwell Changes in benthic denitrification, nitrate ammonification, and anammox process rates and nitrate and nitrite reductase gene abundances along an estuarine nutrient gradient (the Coline Estuary, United Kingdom) Appl. Environ. Microbiol. 75 2009 3171 3179
9. 2 production in coastal marine sediments Geochim. Cosmochim. Acta 69 2005 2057 2065 (Pubitemid 40549401)
10. P. Engstrm, C.R. Penton, and A.H. Devol Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin Limnol. Oceanogr. 54 2009 1643 1652
11. 2 production in a surface flow constructed wetland Environ. Sci. Technol. 42 2008 9144 9150
12. K.F. Ettwig, T. van Alen, K.T. van de Pas-Schoonen, M.S.M. Jetten, and M. Strous Enrichment and molecular detection of denitrifying methanotrophic bacteria in the NC10 phylum Appl. Environ. Microbiol. 75 2009 3656 3662
13. K.F. Ettwig, M.K. Butler, D. Le Paslier, E. Pelletier, S. Mangenot, M.M.M. Kuypers, F. Schreiber, B. Dutilh, J. Zedelius, D. de Beer, J. Gloerich, and H.J.C.T. Wessels Nitrite-driven anaerobic methane oxidation by oxygenic bacteria Nature 464 2010 543 548
14. C.A. Fuchsman, J.W. Murray, and S.K. Konovalov Concentration and natural stable isotope profiles of nitrogen species in the Black Sea Mar. Chem. 111 2008 90 105
15. A. Galn, V. Molina, B. Thamdrup, D. Woebken, G. Lavik, M.M.M. Kuypers, and O. Ulloa Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile Deep-Sea Res. II 56 2009 1021 1031
16. M.R. Hamersley, G. Lavik, D. Woebken, J.E. Rattray, P. Lam, E.C. Hopmans, J.S. Sinninghe Damst, S. Krger, M. Graco, D. Gutirrez, and M.M.M. Kuypers Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone Limnol. Oceanogr. 53 2007 923 933 (Pubitemid 46827143)
17. M.R. Hamersley, D. Woebken, B. Boehrer, M. Schultze, G. Lavik, and M.M.M. Kuypers Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany) Syst. Appl. Microbiol. 32 2009 571 582
18. M. Hanning, G. Lavik, M.M.M. Kuypers, D. Woebken, W. Martens-Habbena, and K. Jurgens Shift from denitrification to anammox after inflow events in the central Baltic Sea Limnol. Oceanogr. 52 2007 1336 1345 (Pubitemid 47121548)
19. S. Hietanen, and J. Kuparinen Seasonal and short-term variation in denitrification and anammox at a coastal station on the Gulf of Finland, Baltic Sea Hydrobiology 596 2008 67 77
20. M.D. Hirsch, Z.T. Long, and B. Song Anammox bacterial diversity in various aquatic ecosystems based on the detection of hydrazine oxidase genes (hzoA/hzoB) Microb. Ecol. 61 2011 264 276
21. + in marine, estuarine, and fresh waters: An adaptation of the ammonia diffusion method for samples with low ammonium concentrations Mar. Chem. 60 1997 235 243 (Pubitemid 28253417)
22. S. Hu, R.J. Zeng, L.C. Burow, P. Lant, J. Keller, and Z. Yuan Enrichment of denitrifying anaerobic methane oxidizing microorganisms Environ. Microbiol. Rep. 1 2009 377 384
23. S. Humbert, S. Tarnawski, N. Fromin, M.-P. Mallet, M. Aragno, and J. Zopfi Molecular detection of anammox bacteria in terrestrial ecosystems: Distribution and diversity ISME J. 4 2010 450 454
24. B. Kartal, M.M. Kuypers, G. Lavik, J. Schalk, H.J.M. Op den Camp, M.S.M. Jetten, and M. Strous Anammox bacteria disguised as denitrifiers: Nitrate reduction to dinitrogen gas via nitrite and ammonium Environ. Microbiol. 9 2007 635 642
25. B. Kartal, J. Rattray, L.A. van Niftrik, J. van de Vossenberg, M.C. Schmid, R.I. Webb, S. Shouten, J.A. Fuerst, J. Sinninghe Damst, M.S.M. Jetten, and M. Strous Candidatus "Anammoxoglobus propionicus" a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria Syst. Appl. Microbiol. 30 2007 39 49 (Pubitemid 44969479)
26. B. Kartal, L. van Niftrik, J. Rattray, J.L.C.M. van de Vossenberg, M.C. Schmid, J.S. Damst, M.S.M. Jetten, and M. Strous Candidatus 'Brocadia fulgida': An autofluorescent anaerobic ammonium oxidizing bacterium FEMS Microbiol. Ecol. 63 2008 46 55 (Pubitemid 350233289)
27. J. Kirkpatrick, B. Oakley, C. Fuchsman, S. Srinivasan, J.T. Staley, and J.W. Murray Diversity and distribution of Planctomycetes and related bacteria in the suboxic zone of the Black Sea Appl. Environ. Microbiol. 72 2006 3079 3083
28. M.G. Klotz, M.C. Schmid, M. Strous, H.J.M. op den Camp, M.S.M. Jetten, and A.B. Hooper Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria Environ. Microbiol. 10 2008 3150 3163
29. S.K. Konovalov, C.A. Fuchsman, V. Belokopitov, and J.W. Murray Modeling the distribution of nitrogen species and isotopes in the water column of the Black Sea Mar. Chem. 111 2008 106 124
30. K. Koop-Jakobsen, and A.E. Giblin Anammox in tidal marsh sediments: The role of salinity, nitrogen loading, and marsh vegetation Estuaries Coasts 32 2009 238 245
31. M.M.M. Kuypers, A.O. Sliekers, G. Lavik, M. Schmid, B.B. Jørgensen, J.G. Kuenen, J. Sinninghe Damst, M. Strous, and M.S.M. Jetten Anaerobic ammonium oxidation by anammox bacteria in the Black Sea Nature 422 2003 608 611 (Pubitemid 36460412)
32. M.M.M. Kuypers, G. Lavik, D. Woebken, M.C. Schmid, B.M. Fuchs, R. Amann, B.B. Jørgensen, and M.S.M. Jetten Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation PNAS 102 2005 6478 6483 (Pubitemid 40617468)
33. P. Lam, M.M. Jensen, G. Lavil, D.F. McGinnis, B. Mller, C.J. Schubert, R. Amann, B. Thamdrup, and M.M.M. Kuypers Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea PNAS 104 2007 7104 7109 (Pubitemid 47186016)
34. P. Lam, G. Lavik, M.M. Jensen, J. van de Vossenberg, M. Schmid, D. Woebken, D. Gutirrez, R. Amann, M.S.M. Jetten, and M.M.M. Kuypers Revising the nitrogen cycle in the Peruvian oxygen minimum zone PNAS 106 2009 4752 4757
35. X.-R. Li, B. Du, H.-X. Fu, R.-F. Wang, J.-H. Shi, Y. Wang, M.S.M. Jetten, and Z.-X. Quan The bacterial diversity in an anaerobic ammonium-oxidizing (anammox) reactor community Syst. Appl. Microbiol. 32 2009 278 289
36. H. Li, S. Chen, B.-Z. Mu, and J.-D. Gu Molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in high-temperature petroleum reservoirs Microb. Ecol. 60 2010 771 783
37. M. Li, Y. Hong, M.G. Klotz, and J.-D. Gu A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments Appl. Microbiol. Biotechnol. 86 2010 781 790
38. W. Ludwing, G. Kirchof, N. Klugbauer, M. Weizenegger, D. Betzl, M. Ehrmann, C. Hertel, S. Jilg, R. Tatzel, H. Zitzelsberger, S. Lerbl, and J. Hochberger Complete 23S ribosomal RNA sequences of gram-positive bacteria with a low G + C content Syst. Appl. Microbiol. 15 1992 487 501 (Pubitemid 23036061)
39. M. McIlvin, and K.L. Casciotti Fully automated system for stable isotopic analysis of dissolved nitrous oxide at natural abundance levels Limnol. Oceanogr. Methods 8 2010 54 66
40. R.L. Meyer, N. Rigaard-Petersen, and D.E. Allen Correlation between anammox activity and microscale distribution of nitrite in subtrophical mangrove sediment Appl. Environ. Microbiol. 71 2005 6142 6149 (Pubitemid 41456912)
41. L. Minjeaud, P.C. Bonin, and V.D. Michotey Nitrogen fluxes from marine sediments:quantification of the associated co-occurring bacterial processes Biogeochemistry 90 2008 141 157
42. A. Mulder, A.A. van de Graaf, L.A. Robertson, and J.G. Kuenen Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor FEMS Microbiol. Ecol. 16 1995 177 184
43. A. Neef, R.I. Amann, H. Schlesner, and K.-H. Schleifer Monitoring a widespread bacterial group: in situ detection of Planctomycetes with 16S rRNA-targeted probes Microbiol. 144 1998 3257 3266 (Pubitemid 29011955)
44. D.B. Nedwell, T.D. Jickells, M. Trimmer, and R. Sanders Nutrients in estuaries D.B. Nedwell, D.G. Raffaelli, Estuaries, Advances in Ecological Research, Vol. 29 1999 Academic Press London 43 92
45. J.C. Nicholls, and M. Trimmer Widespread occurrence of the anammox reaction in estuarine sediments Aquat. Microb. Ecol. 55 2009 105 113
46. G.J. Olsen, D.J. Lane, S.J. Giovannoni, N.R. Pace, and D.A. Stahl Microbial Ecology and Evolution: A Ribosomal Approach Annual Rev. Microbiol. 40 1986 337 365
47. M. Pavlekovic, M.C. Schmid, N. Schmider-Poignee, S. Spring, M. Philhofer, T. Gaul, M. Fiandaca, F.E. Lffler, M. Jetten, K.-H. Schleifer, and N.M. Lee Optimization of three FISH procedures for in situ detection of anaerobic ammonium oxidizing bacteria in biological wastewater treatment J. Microbiol. Methods 78 2009 119 126
48. C.R. Penton, A.H. Devol, and J.M. Tiedje Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments Appl. Environ. Microbiol. 72 2006 6829 6832 (Pubitemid 44582930)
49. M.G. Propenko, D.E. Hammond, W.M. Berelson, J.M. Bernhard, L. Stott, and R. Douglas Nitrogen cycling in the sediments of Santa Barabara basin and Eastern Subtropical North Pacific: Nitrogen isotopes, diagenesis, and possible chemosymbiosis between two lithotrophs (Thioploca and Anammox)" riding on a glider" Earth Planet. Sci. Lett. 242 2006 186 204 (Pubitemid 43138005)
50. Z.-X. Quan, S.-K. Rhee, J.-E. Zuo, Y. Yang, J.-W. Bae, J.R. Park, S.-T. Lee, and Y.-H. Park Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor Environ. Microbiol. 10 2008 3130 3139
51. A.A. Raghoebarsing, A. Pol, K.T. van de Pas-Schoonen, A.J.P. Smolders, K.F. Ettwig, I.C. Rijpstra, S. Schouten, J.S.S. Damst, H.J.M. Op den Camp, M.S.M. Jetten, and M. Strous A microbial consortium couples anaerobic methane oxidation to denitrification Nature 440 2006 918 921
52. J.J. Rich, O.R. Dale, B. Song, and B.B. Ward Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments Microb. Ecol. 53 2008 311 320 (Pubitemid 351171471)
53. N.S. Risgaard-Petersen, S. Rysgaard, and N.P. Revsbech Combined microdiffusion-hypobromite oxidation method for determining nitrogen-15 isotope in ammonium Soil Sci. Soc. Am. J. 59 1995 1077 1080 (Pubitemid 26438890)
54. N. Risgaard-Petersen, L.P. Nielsen, S. Rysgaard, T. Dalsgaard, and R.L. Meyer Application of the isotope pairing technique in sediments where anammox and denitrification co-exist Limnol. Oceanogr. Methods 1 2003 63 73
55. N. Risgaard-Petersen, R.L. Meyer, M. Schmid, M.S.M. Jetten, A. Enrich-Prast, S. Rysgaard, and N.P. Revsbech Anaerobic ammonium oxidation in an estuarine sediment Aquat. Microb. Ecol. 36 2004 293 304 (Pubitemid 39393898)
56. N. Risgaard-Petersen, L.P. Nielsen, S. Rysgaard, T. Dalsgaard, and R.L. Meyer Erratum: Application of the isotope pairing technique in sediments where anammox and denitrification co-exist Limnol. Oceanogr. Methods 2 2004 315 (Pubitemid 43723700)
57. J. Schalk, S. de Vries, G. Kuenen, and M.S.M. Jetten Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation Biochemistry 39 2000 5405 5412 (Pubitemid 30257081)
58. M.C. Schmid, U. Twachtmann, M. Klein, M. Strous, S. Juretschko, M.S.M. Jetten, J.W. Metzger, K.H. Schleifer, and M. Wagner Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation Syst. Appl. Microbiol. 23 2000 93 106 (Pubitemid 30237496)
59. M.C. Schmid, S. Schmitz-Esser, M.S.M. Jetten, and M. Wagner 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium oxidizers: Implications for phylogeny and in situ detection Environ. Microbiol. 3 2001 450 459 (Pubitemid 33136729)
60. M.C. Schmid, K. Walsh, R. Webb, W.I. Rijpstra, K. van de Pas-Schoonen, M.J. Verbruggen, T. Hill, B. Moffett, J. Fuerst, S. Schouten, J.S. Damst, and J. Harris Candidatus "Scalindua brodae", sp. Nov., Candidatus "Scalindua wagneri", sp. Nov., two new species of anaerobic ammonium oxidizing bacteria Syst. Appl. Microbiol. 26 2003 529 538 (Pubitemid 37486511)
61. M.C. Schmid, B. Maas, A. Dapena, K. van de Pas-Schoonen, J. van de Vossenberg, B. Kartal, L. van Niftrik, I. Schmidt, I. Cirpus, J.G. Kuenen, M. Wagner, and J.S. Sinninghe Damst Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria Appl. Environ. Microbiol. 71 2005 1677 1684 (Pubitemid 40552872)
62. M.C. Schmid, N. Risgaard-Petersen, J. van de Vossenberg, M.M.M. Kuypers, G. Lavik, J. Petersen, S. Hulth, B. Thamdrup, D. Canfield, T. Dalsgaard, S. Rysgaard, and M.K. Sejr Anaerobic ammonium-oxidizing bacteria in marine environments: Widespread occurrence but low diversity Environ. Microbiol. 9 2007 1476 1484 (Pubitemid 46763528)
63. M.C. Schmid, A.B. Hooper, M.G. Klotz, D. Woebken, P. Lam, M.M.M. Kuypers, A. Pommerening-Roeser, H.J.M. op den Camp, and M.S.M. Jetten Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria Environ. Microbiol. 10 2008 3140 3149
64. C.J. Schubert, E. Durisch-Kaiser, B. Wehrli, B. Thamdrup, P. Lam, and M.M.M. Kuypers Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika) Environ. Microbiol. 10 2006 1857 1863 (Pubitemid 44326477)
65. S.P. Seitzinger Linkages between organic matter mineralization and denitrification in eight riparian wetlands Biogeochemistry 25 1994 19 39 (Pubitemid 2110316)
66. S.P. Seitzinger, and A. Giblin Estimating denitrification in North Atlantic continental shelf sediments Biogeochemistry 35 1996 235 260
67. S.P. Seitzinger, J.A. Harrison, J.K. Bhlke, A.F. Bouwman, R. Lowrance, B. Peterson, C. Tobias, and G. Van Drecht Denitrification across landscapes and waterscapes: A synthesis Ecol. Applic. 16 2006 2064 2090 (Pubitemid 44917572)
68. M. Shimamura, T. Nishiyama, H. Shigetomo, T. Toyomoto, Y. Kawahara, K. Furukawa, and F. Takao Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture Appl. Environ. Microbiol. 73 2007 1065 1072
69. D.M. Sigman, M.A. Altabet, R. Michener, D.C. McCorkle, B. Fry, and R.M. Holmes Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: An adaptation of the ammonium diffusion method Mar. Chem. 57 1997 227 242 (Pubitemid 27369728)
70. D.M. Sigman, K.L. Casciotti, M. Andreani, C. Barford, M. Galanter, and J.K. Bhlke A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater Anal. Chem. 73 2001 4145 4153 (Pubitemid 32830853)
71. J. Sørenson Nitrate reduction in marine sediment: Pathways and interactions with iron and sulfur cycling Geomicrobiol. J. 5 1987 401 422
72. M. Strous, J.J. Heijen, J.G. Kuenen, and M.S.M. Jetten 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 (Pubitemid 28555299)
73. M. Strous, E. Pelletier, S. Magenot, T. Rattei, A. Lehner, M.W. Taylor, M. Horn, H. Daims, D. Bartol-Marvel, P. Wincker, V. Barbe, and N. Fonknechten Deciphering the evolution and metabolism of an anammox bacterium from a community genome Nature 440 2006 790 794
74. 2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments Appl. Environ. Microbiol. 68 2002 1312 1318 (Pubitemid 34205371)
75. B. Thamdrup, T. Dalsgaard, M.S.M. Jensen, O. Ulloa, L. Farias, and R. Escribano Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile Limnol. Oceanogr. 51 2006 2145 2156 (Pubitemid 44520911)
76. C.R. Tobias, S.A. Macko, I.C. Anderson, E.A. Canuel, and J.W. Harvey Tracking the fate of a high concentration groundwater nitrate plume through a fringing marsh: A combined groundwater tracer and in situ isotope enrichment study Limnol. Oceanogr. 46 2001 1977 1989 (Pubitemid 34009947)
77. M. Trimmer, and J.C. Nicholls Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic Limnol. Oceanogr. 54 2009 577 589
78. M. Trimmer, J.C. Nicholls, and B. Deflandre Anaerobic ammonium oxidation measured in sediments along the Thames Estuary, United Kingdom Appl. Environ. Microbiol. 69 2003 6447 6454 (Pubitemid 37420176)
79. M. Trimmer, J.C. Nicholls, C. Morely, C.A. Davies, and J. Aldrigde Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment Appl. Environ. Microbiol. 71 2005 1923 1930 (Pubitemid 40546113)
80. M. Trimmer, Nicholls Risgaard-Petersen, and P. Engstrm Direct measurement of anaerobic ammonium oxidation (anammox) and denitrification in intact sediment cores Mar. Ecol. Prog. Ser. 326 2006 37 47 (Pubitemid 46026123)
81. A.A. van de Graaf, A. Mulder, P. de Bruijn, M.S.M. Jetten, L.A. Robertson, and J.G. Kuenen Anaerobic oxidation of ammonium is a biologically mediated process Appl. Environ. Microbiol. 61 1995 1246 1251
82. B.B. Ward, A.H. Devol, J.J. Rich, B.X. Chang, S.E. Bulow, H. Naik, A. Pratihary, and A. Jayakumar Denitrification as the dominant nitrogen loss process in the Arabian Sea Nature 461 2009 78 81
83. D. Woebken, P. Lam, M.M.M. Kuypers, S.W.A. Naqvi, B. Kartal, M. Strous, M.S.M. Jetten, B.M. Fuchs, and R. Amann A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones Environ. Microbiol. 10 2008 3106 3119
84. S. Yoshie, N. Noda, S. Tsuneda, A. Hirata, and Y. Inamori Salinity decreases nitrate reductase gene diversity in denitrifying bacteria of wastewater treatment systems Appl. Environ. Microbiol. 70 2004 3152 3157 (Pubitemid 38657839)