Advances in methods for detection of anaerobic ammonium oxidizing (anammox) bacteria

Applied Microbiology and Biotechnology

Volumn 90, Issue 4, 2011, Pages 1241-1252

  Li, Meng ^a   Gu, Ji Dong ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

16S rRNA gene; Anammox bacteria; Functional biomarkers; Isotope pairing technique; Lipid analysis; Molecular technique

Indexed keywords

16S RRNA GENE; ANAMMOX; FUNCTIONAL BIOMARKERS; ISOTOPE PAIRING TECHNIQUE; LIPID ANALYSIS; MOLECULAR TECHNIQUES;

AMMONIUM COMPOUNDS; BACTERIOLOGY; CHEMICAL DETECTION; GENE ENCODING; ISOTOPES; NITROGEN; POLYMERASE CHAIN REACTION; RNA; TRANSCRIPTION; WASTEWATER TREATMENT;

NITROGEN REMOVAL;

RNA 16S;

AMMONIUM; BACTERIUM; BIOCHEMICAL COMPOSITION; BIOCHEMISTRY; BIOMARKER; DETECTION METHOD; ELECTRON; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; ISOTOPIC ANALYSIS; LIPID; NITRITE; NITROGEN CYCLE; OXIDATION; PHYSIOLOGICAL RESPONSE; POLYMERASE CHAIN REACTION; STABLE ISOTOPE;

ANAEROBIC AMMONIUM OXIDATION; ANAEROBIC METABOLISM; BACTERIUM DETECTION; BIOMASS DISTRIBUTION; CONTROLLED STUDY; DENITRIFICATION; DNA DETERMINATION; DNA SEQUENCE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; INTERMETHOD COMPARISON; ISOTOPE LABELING; ISOTOPE PAIRING TECHNIQUE; LIPID ANALYSIS; MASS FRAGMENTOGRAPHY; MOLECULAR BIOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; REVIEW; RNA EXTRACTION; TANDEM MASS SPECTROMETRY;

ANAEROBIOSIS; BACTERIA; BACTERIOLOGICAL TECHNIQUES; ENVIRONMENTAL MICROBIOLOGY; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; QUATERNARY AMMONIUM COMPOUNDS;

EID: 79955564819     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-011-3230-6     Document Type: Review

References (101)

1. RI Amann L Krumholz DA Stahl 1990 Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology J Bacteriol 172 762 770 1:CAS:528:DyaK3cXhtFGmtb0%3D (Pubitemid 20070387)
2. RI Amann W Ludwig KH Schleifer 1995 Phylogenetic identification and in situ detection of individual microbial cells without cultivation Microbiol Rev 59 143 169 1:CAS:528:DyaK2MXkvVGmurk%3D
3. H Bae K Park Y Chung J Jung 2010 Distribution of anammox bacteria in domestic WWTPs and their enrichments evaluated by real-time quantitative PCR Process Biochem 45 323 334 10.1016/j.procbio.2009.10.004 1:CAS:528: DC%2BC3cXhtVamu7Y%3D
4. HA Boumann EC Hopmans I van de Leemput HJM Camp J van de Vossenberg M Strous MSM Jetten JS Sinninghe Damsté S Schouten 2006 Ladderane phospholipids in anammox bacteria comprise phosphocholine and phosphoethanolamine headgroups FEMS Microbiol Lett 258 297 304 10.1111/j.1574-6968.2006.00233.x 1:CAS:528:DC%2BD28XltV2jsrc%3D
5. J Brandsma J van de Vossenberg N Risgaard-Petersen MC Schmid P Engstrom K Eurenius S Hulth A Jaeschke B Abbas EC Hopmans M Strous S Schouten MSM Jetten JS Sinninghe Damsté 2011 A multi-proxy study of anaerobic ammonium oxidation in marine sediments of the Gullmar Fjord, Sweden Environ Microbiol Rep 10.111/j.1758-2229.2010.00233.x
6. ID Bull NR Parekh GH Hall P Ineson RP Evershed 2000 Detection and classification of atmospheric methane oxidizing bacteria in soil Nature 405 175 178 10.1038/35012061 1:CAS:528:DC%2BD3cXjsFOqsbs%3D (Pubitemid 30313533)
7. N Byrne M Strous V Crepeau B Kartal JL Birrien M Schmid F Lesongeur S Schouten A Jaeschke M Jetten D Prieur A Godfroy 2009 Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents ISME J 3 117 123 10.1038/ismej.2008.72 1:CAS:528:DC%2BD1MXms12gtr8%3D
8. T Dalsgaard B Thamdrup 2002 Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments Appl Environ Microbiol 68 3802 3808 10.1128/AEM.68.8.3802-3808.2002 1:CAS:528:DC%2BD38XmtVaquro%3D (Pubitemid 34836688)
9. 2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica Nature 422 606 608 10.1038/nature01526 1:CAS:528:DC%2BD3sXislCgtLs%3D (Pubitemid 36460411)
10. T Dalsgaard B Thamdrup DE Canfield 2005 Anaerobic ammonium oxidation (anammox) in the marine environment Res Microbiol 156 457 464 10.1016/j.resmic.2005.01.011 1:CAS:528:DC%2BD2MXjvVOjtbs%3D (Pubitemid 40615411)
11. Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434-444
12. H Dang R Chen L Wang L Guo P Chen Z Tang F Tian S Li MG Klotz 2010 Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China Appl Environ Microbiol 76 7036 7047 10.1128/AEM.01264-10 1:CAS:528:DC%2BC3MXkvVGg
13. TE Davidsson R Stepanauskas L Leonardson 1997 Vertical patterns of nitrogen transformations during infiltration in two wetland soils Appl Environ Microbiol 63 3648 3656 1:CAS:528:DyaK2sXmtVKhur0%3D (Pubitemid 27383166)
14. AH Devol 2003 Nitrogen cycle-solution to a marine mystery Nature 422 575 576 10.1038/422575a 1:CAS:528:DC%2BD3sXislCgtrc%3D (Pubitemid 36460400)
15. X Dong EW Tollner 2003 Evaluation of Anammox and denitrification during anaerobic digestion of poultry manure Bioresour Technol 86 139 145 10.1016/S0960-8524(02)00154-2 1:CAS:528:DC%2BD38XnvVKjtL8%3D
16. CA Francis JM Beman MM Kuypers 2007 New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation ISME J 1 19 27 10.1038/ismej.2007.8 1:CAS:528:DC%2BD1cXksFSgu7o%3D (Pubitemid 46717128)
17. SJ Giovannoni EF Delong GJ Olsen NR Pace 1988 Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial cells J Bacteriol 170 720 726 1:CAS:528:DyaL1cXktF2lsbY%3D
18. Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, Damsté JSS, Krüger S, Graco M, Gutierrez D, Kuypers MMM (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52:923-933
19. C Hellinga AAJC Schellen JW Mulder MCM van Loosdrecht JJ Heijnen 1998 The SHARON process: an innovative method for nitrogen removal from ammonium-rich waste water Water Sci Technol 37 9 135 142 10.1016/S0273-1223(98)00281-9 1:CAS:528:DyaK1cXls1Oit7o%3D (Pubitemid 28383347)
20. Hirsch MD, Long ZT, Song B (2011) Anammox bacterial diversity in various aquatic ecosystems based on the detection of hydrazine oxidase genes (hzoA/hzoB). Microb Ecol 61:264-267
21. Hong YG, Li M, Cao HL, Gu J-D (2011) Residence of habitat-specific anammox bacteria in the deep-sea subsurface sediments of South China Sea: analyses of maker gene abundance context with physicochemical parameters. Microb Ecol. doi: 10.1007/s00248-011-9849-0
22. Hong YG, Yin B, Zheng TL (2011a) Diversity and abundance of anammox bacterial community in the deep-ocean surface sediment from equatorial Pacific. Appl Microbiol Biotechnol 89:1233-1241
23. EC Hopmans MVM Kienhuis JE Rattray A Jaeschke S Schouten JSS Damste 2006 Improved analysis of ladderane lipids in biomass and sediments using high-performance liquid chromatography/atmospheric pressure chemical ionization tandem mass spectrometry Rapid Commun Mass Spectrom 20 2099 2103 10.1002/rcm.2572 1:CAS:528:DC%2BD28XnsVOqsbs%3D (Pubitemid 44049035)
24. T Hoshino LS Yilmaz DR Noguera H Daims M Wagner 2008 Quantification of target molecules needed to detect microorganisms by fluorescence in situ hybridization (FISH) and catalyzed reporter deposition-FISH Appl Environ Microbiol 74 5068 5077 10.1128/AEM.00208-08 1:CAS:528:DC%2BD1cXhtVehu7nF
25. A Jaeschke EC Hopmans SG Wakeham S Schouten JSS Damste 2007 The presence of ladderane lipids in the oxygen minimum zone of the Arabian Sea indicates nitrogen loss through anammox Limnol Oceanogr 52 780 786 10.4319/lo.2007.52.2. 0780 1:CAS:528:DC%2BD2sXkt1Wgs7o%3D (Pubitemid 46972312)
26. A Jaeschke C Rooks M Trimmer JC Nicholls EC Hopmans S Schouten JS Sinninghe Damsté 2009 Comparison of ladderane phospholipids and core lipids as indicators for anaerobic ammonium oxidation (anammox) in marine sediments Geochim Cosmochim Acta 73 2077 2088 10.1016/j.gca.2009.01.013 1:CAS:528:DC%2BD1MXjtFamtro%3D
27. MSM Jetten MC Schmid I Schmidt M Wubben U van Dongen W Abma AO Sliekers NP Revsbech HJE Beaumont L Ottosen E Volcke HJ Laanbroek JL Campos Gomez JA Cole MCM van Loosdrecht JW Mulder J Fuerst D Richardson KT van de Pas-Schoonen R Mendez Pampin K Third K Cirpus R van Spanning A Bollmann LP Nielsen HJM Op den Camp JGC Schultz P Vanrolleghem M Strous M Wagner JG Kuenen 2002 Improved nitrogen removal by application of new nitrogen-cycle bacteria Rev Environ Sci Biotechnol 1 51 63 10.1023/A:1015191724542 1:CAS:528:DC%2BD38Xltleksb8%3D
28. Jetten MSM, Sliekers O, Kuypers M, Dalsgaard T, van Niftrik L, Cirpus I, van de Pas-Schoonen K, Lavik G, Thamdrup B, Le Paslier D, Op den Camp HJM, Hulth S, Nielsen LP, Abma W, Third K, Engstrom P, Kuenen JG, Jorgensen BB, Canfield DE, Damsté JSS, Revsbech NP, Fuerst J, Weissenbach J, Wagner M, Schmidt I, Schmid M, Strous M (2003) Anaerobic ammonium oxidation by marine and freshwater planctomycete-like bacteria. Appl Microbiol Biotechnol 63:107-114
29. M Jetten M Schmid K van de Pas-Schoonen J Sinninghe Damste M Strous 2005 Anammox organisms: enrichment, cultivation, and environmental analysis Methods Enzymol 397 34 57 10.1016/S0076-6879(05)97003-1 1:CAS:528:DC%2BD2sXlvFymur4%3D (Pubitemid 41562893)
30. MS Jetten L Niftrik M Strous B Kartal JT Keltjens HJ Op den Camp 2009 Biochemistry and molecular biology of anammox bacteria Crit Rev Biochem Mol Biol 44 65 84 1:CAS:528:DC%2BD1MXlslWiu7Y%3D
31. P Junier V Molina C Dorador O Hadas OS Kim T Junier JP Witzel JF Imhoff 2010 Phylogenetic and functional marker genes to study ammonia-oxidizing microorganisms (AOM) in the environment Appl Microbiol Biotechnol 85 425 440 10.1007/s00253-009-2228-9 1:CAS:528:DC%2BC3cXit1OrtQ%3D%3D
32. J Kallmeyer DC Smith 2009 An improved electro-elution method for separation of DNA from humic substances in marine sediment DNA extracts FEMS Microbiol Ecol 69 125 131 10.1111/j.1574-6941.2009.00684.x 1:CAS:528: DC%2BD1MXnslGitLg%3D
33. B Kartal MM Kuypers G Lavik J Schalk HJ Op den Camp MS Jetten M Strous 2007 Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium Environ Microbiol 9 635 642 10.1111/j.1462-2920. 2006.01183.x 1:CAS:528:DC%2BD2sXjs1Gms7k%3D
34. B Kartal J Rattray LA van Niftrik J van de Vossenberg MC Schmid RI Webb S Schouten JA Fuerst JS Damste MS Jetten M Strous 2007 Candidatus "Anammoxoglobus propionicus" a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria Syst Appl Microbiol 30 39 49 10.1016/j.syapm.2006.03.004 1:CAS:528:DC%2BD2sXjt1SntLc%3D (Pubitemid 44969479)
35. B Kartal L van Niftrik J Rattray JL van de Vossenberg MC Schmid J Sinninghe Damste MS Jetten M Strous 2008 Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium FEMS Microbiol Ecol 63 46 55 10.1111/j.1574-6941.2007.00408.x 1:CAS:528:DC%2BD1cXhvVOnurc%3D (Pubitemid 350233289)
36. B Kartal W Geerts MS Jetten 2011 Cultivation, detection, and ecophysiology of anaerobic ammonium-oxidizing bacteria Methods Enzymol 486 89 108 10.1016/B978-0-12-381294-0.00004-3 1:CAS:528:DC%2BC3MXjtVSltr8%3D
37. MG Klotz MC Schmid M Strous HJ Op den Camp MS Jetten AB Hooper 2008 Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria Environ Microbiol 10 3150 3163 10.1111/j.1462-2920.2008.01733.x 1:CAS:528:DC%2BD1cXhtlGitrfJ
38. LP Kuai W Verstraete 1998 Ammonium removal by the oxygen-limited autotrophic nitrification-denitrification system Appl Environ Microbiol 64 4500 4506 1:CAS:528:DyaK1cXnt1ajtLk%3D (Pubitemid 28538025)
39. K Kubota A Ohashi H Imachi H Harada 2006 Improved in situ hybridization efficiency with locked-nucleic-acid-incorporated DNA probes Appl Environ Microbiol 72 5311 5317 10.1128/AEM.03039-05 1:CAS:528:DC%2BD28XosVKls7o%3D
40. JG Kuenen 2008 Anammox bacteria: from discovery to application Nat Rev Microbiol 6 320 326 10.1038/nrmicro1857 1:CAS:528:DC%2BD1cXjt1Cqur4%3D (Pubitemid 351404776)
41. M Kumar J-G Lin 2010 Co-existence of anammox and denitrification for simultaneous nitrogen and carbon removal-strategies and issues J Hazard Mater 178 1 9 10.1016/j.jhazmat.2010.01.077 1:CAS:528:DC%2BC3cXksV2qt74%3D
42. MM Kuypers AO Sliekers G Lavik M Schmid BB Jorgensen JG Kuenen JS Sinninghe Damste M Srous MS Jetten 2003 Anaerobic ammonium oxidation by anammox bacteria in the Black Sea Nature 422 608 611 10.1038/nature01472 1:CAS:528:DC%2BD3sXislCgt7Y%3D (Pubitemid 36460412)
43. MM Kuypers G Lavik D Woebken M Schmid BM Fuchs R Amann BB Jorgensen MS Jetten 2005 Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation Proc Natl Acad Sci USA 102 6478 6483 10.1073/pnas.0502088102 1:CAS:528:DC%2BD2MXktlygtLs%3D (Pubitemid 40617468)
44. P Lam G Lavik MM Jensen J van de Vossenberg M Schmid D Woebken D Gutierrez R Amann MS Jetten MM Kuypers 2009 Revising the nitrogen cycle in the Peruvian oxygen minimum zone Proc Natl Acad Sci USA 106 4752 4757 10.1073/pnas.0812444106 1:CAS:528:DC%2BD1MXktFOgtLY%3D
45. N Lee PH Nielsen KH Andreasen S Juretschko JL Nielsen KH Schleifer M Wagner 1999 Combination of fluorescent in situ hybridization and microautoradiography - a new tool for structure-function analyses in microbial ecology Appl Environ Microbiol 65 1289 1297 1:CAS:528:DyaK1MXhslWku7k%3D
46. XR Li B Du HX Fu RF Wang JH Shi Y Wang MS Jetten ZX Quan 2009 The bacterial diversity in an anaerobic ammonium-oxidizing (anammox) reactor community Syst Appl Microbiol 32 278 289 10.1016/j.syapm.2009.03.002 1:CAS:528:DC%2BD1MXosVygtLg%3D
47. H Li S Chen BZ Mu J-D Gu 2010 Molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in high-temperature petroleum reservoirs Microb Ecol 60 771 783 10.1007/s00248-010-9733-3 1:CAS:528:DC%2BC3cXhtlyrsrbI
48. M Li Y Hong MG Klotz J-D Gu 2010 A comparison of primer sets for detecting 16S rRNA and hydrazine oxidoreductase genes of anaerobic ammonium-oxidizing bacteria in marine sediments Appl Microbiol Biotechnol 86 781 790 10.1007/s00253-009-2361-5 1:CAS:528:DC%2BC3cXit1amsb8%3D
49. Li M, Cao H, Hong Y, Gu J-D (2011a) Seasonal dynamics of anammox bacteria in estuarial sediment of the Mai Po Nature Reserve revealed by analyzing the 16S rRNA and hydrazine oxidoreductase (hzo) genes. Microb Environ 26:15-22
50. Li M, Ford T, Li XY, Gu J-D (2011b) Cytochrome cd-1-containing nitrite encoding gene nirS as a new functional biomarker for detection of anaerobic ammonium oxidizing (Anammox) bacteria. Envion Sci Technol. doi: 10.1021/es103826w
51. E Lindberg HJ Albrechtsen CS Jacobsen 2007 Inhibition of real-time PCR in DNA extracts from aquifer sediment Geomicrobiol J 24 343 352 10.1080/01490450701456701 1:CAS:528:DC%2BD2sXotV2rtbs%3D (Pubitemid 47180063)
52. C Moraru P Lam BM Fuchs MM Kuypers R Amann 2010 GeneFISH-an in situ technique for linking gene presence and cell identity in environmental microorganisms Environ Microbiol 12 3057 3073 10.1111/j.1462-2920.2010.02281.x 1:CAS:528:DC%2BC3cXhsFyrsrbF
53. E Morgenroth A Obermayer E Arnold A Brühl M Wagner PA Wilderer 2000 Effect of long-term idle periods on the performance of sequencing batch reactors Water Sci Technol 41 105 113 1:CAS:528:DC%2BD3cXhsF2ku7Y%3D (Pubitemid 30093847)
54. Murrell JC, Whiteley A (2011) Stable isotope probing and related technologies. ASM, Washington
55. Neef A, Amann R, Schlesner H, Schleifer KH (1998) Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 144:3257-3266 (Pubitemid 29011955)
56. BJ Ni BL Hu F Fang WM Xie B Kartal XW Liu GP Sheng M Jetten P Zheng HQ Yu 2010 Microbial and physicochemical characteristics of compact anaerobic ammonium-oxidizing granules in an upflow anaerobic sludge blanket reactor Appl Environ Microbiol 76 2652 2656 10.1128/AEM.02271-09 1:CAS:528: DC%2BC3cXlsVSlsLs%3D
57. LP Nielsen 1992 Denitrification in sediments determined from nitrogen isotope pairing FEMS Microbiol Ecol 86 357 362 10.1111/j.1574-6968.1992.tb04828. x 1:CAS:528:DyaK38Xit1Wjsr8%3D
58. H Park A Rosenthal K Ramalingam J Fillos K Chandran 2010 Linking community profiles, gene expression and N-removal in anammox bioreactors treating municipal anaerobic digestion reject water Environ Sci Technol 44 6110 6116 10.1021/es1002956 1:CAS:528:DC%2BC3cXovFegs7o%3D
59. M Pavlekovic MC Schmid N Schmider-Poignee S Spring M Pilhofer T Gaul M Fiandaca FE Löffler M Jetten KH Schleifer NM Lee 2009 Optimization of three FISH procedures for in situ detection of anaerobic ammonium oxidizing bacteria in biological wastewater treatment J Microbiol Methods 78 119 126 10.1016/j.mimet.2009.04.003 1:CAS:528:DC%2BD1MXoslCmsrs%3D
60. CR Penton AH Devol JM Tiedje 2006 Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments Appl Environ Microbiol 72 6829 6832 10.1128/AEM.01254-06 1:CAS:528:DC%2BD28XhtFalsLbN (Pubitemid 44582930)
61. A Pernthaler J Pernthaler R Amann 2002 Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria Appl Environ Microbiol 68 3094 3101 10.1128/AEM.68.6.3094-3101.2002 1:CAS:528:DC%2BD38XksVWqtL0%3D (Pubitemid 34602035)
62. H Perry-O'Keefe S Rigby K Oliveira D Sorensen H Stender J Coull JJ Hyldig-Nielsen 2001 Identification of indicator microorganisms using a standardized PNA FISH method J Microbiol Methods 47 281 292 10.1016/S0167- 7012(01)00303-7 (Pubitemid 33063645)
63. - consumption in a Danish lowland stream: diurnal and seasonal variation Aquat Microb Ecol 12 275 284 10.3354/ame012275 (Pubitemid 127471726)
64. LK Poulsen G Ballard DA Stahl 1993 Use of rRNA fluorescence in situ hybridization for measuring the activity of single cells in young and established biofilms Appl Environ Microbiol 59 1354 1360 1:CAS:528: DyaK3sXks1Chs7k%3D (Pubitemid 23141141)
65. 2 fixation by archaea and bacteria in an agricultural soil Proc Natl Acad Sci USA 10.1073/pnas.1010981108
66. ZX Quan SK Rhee JE Zuo Y Yang JW Bae JR Park ST Lee YH Park 2008 Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor Environ Microbiol 10 3130 3139 10.1111/j.1462-2920.2008.01642.x 1:CAS:528:DC%2BD1cXhtlGitrfP
67. N Risgaard-Petersen 2003 Coupled nitrification-denitrification in autotrophic and heterotrophic estuarine sediments: on the influence of benthic microalgae Limnol Oceanogr 48 93 105 10.4319/lo.2003.48.1.0093 1:CAS:528:DC%2BD3sXhtVGrurw%3D (Pubitemid 36154247)
68. N Risgaard-Petersen LP Nielsen S Rysgaard T Dalsgaard RL Meyer 2003 Application of the isotope pairing technique in sediments where anammox and denitrification coexist Limnol Oceanogr: Methods 1 63 73 10.4319/lom.2011.1.63
69. N Risgaard-Petersen RL Meyer M Schmid MSM Jetten A Enrich-Prast S Rysgaard NP Revsbech 2004 Anaerobic ammonium oxidation in an estuarine sediment Aquat Microb Ecol 36 293 304 10.3354/ame036293 (Pubitemid 39393898)
70. 2 production in Arctic sea ice Limnol Oceanogr 49 86 94 10.4319/lo.2004.49.1.0086 1:CAS:528: DC%2BD2cXhsVelt78%3D (Pubitemid 38154289)
71. 15N dilution technique and isotope pairing Appl Environ Microbiol 59 2093 2098 1:CAS:528:DyaK3sXls1Ohsrg%3D
72. S Rysgaard RN Glud N Risgaard-Petersen T Dalsgaard 2004 Denitrification and anammox activity in Arctic marine sediments Limnol Oceanogr 49 1493 1502 10.4319/lo.2004.49.5.1493 1:CAS:528:DC%2BD2cXovVWqs7g%3D (Pubitemid 39320744)
73. M Schmid U Twachtmann M Klein M Strous S Juretschko M Jetten JW Metzger KH Schleifer M Wagner 2000 Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation Syst Appl Microbiol 23 93 106 1:CAS:528:DC%2BD3cXksFShsbY%3D (Pubitemid 30237496)
74. M Schmid S Schmitz-Esser M Jetten M Wagner 2001 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium-oxidizing bacteria: implications for phylogeny and in situ detection Environ Microbiol 3 450 459 10.1046/j.1462-2920. 2001.00211.x 1:CAS:528:DC%2BD3MXntVOjs7o%3D (Pubitemid 33136729)
75. M Schmid K Walsh R Webb WIC Rijpstra K van de Pas-Schoonen MJ Verbruggen T Hill B Moffett J Fuerst S Schouten JSS Damste J Harris P Shaw M Jetten M Strous 2003 Candidatus "Scalindua brodae", sp. nov., Candidatus "Scalindua wagneri", sp. nov., two new species of anaerobic ammonium oxidizing bacteria Syst Appl Microbiol 26 529 538 10.1078/072320203770865837 1:CAS:528:DC%2BD2cXls1OltQ%3D%3D (Pubitemid 37486511)
76. MC Schmid B Maas A Dapena K van de Pas-Schoonen J van de Vossenberg B Kartal L van Niftrik I Schmidt I Cirpus JG Kuenen M Wagner JS Sinninghe Damste M Kuypers NP Revsbech R Mendez MS Jetten M Strous 2005 Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria Appl Environ Microbiol 71 1677 1684 10.1128/AEM.71.4.1677-1684.2005 1:CAS:528: DC%2BD2MXjsVOqtro%3D (Pubitemid 40552872)
77. MC Schmid N Risgaard-Petersen J van de Vossenberg MMM Kuypers G Lavik J Petersen S Hulth B Thamdrup D Canfield T Dalsgaard S Rysgaard MK Sejr M Strous HJ den Camp MS Jetten 2007 Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity Environ Microbiol 9 1476 1484 10.1111/j.1462-2920.2007.01266.x 1:CAS:528:DC%2BD2sXnt1GlsLw%3D (Pubitemid 46763528)
78. MC Schmid AB Hooper MG Klotz D Woebken P Lam MM Kuypers A Pommerening-Roeser HJ Op den Camp MS Jetten 2008 Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria Environ Microbiol 10 3140 3149 10.1111/j.1462-2920.2008.01732.x 1:CAS:528:DC%2BD1cXhtlGitrfI
79. CJ Schubert E Durisch-Kaiser B Wehrli B Thamdrup P Lam MM Kuypers 2006 Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika) Environ Microbiol 8 1857 1863 10.1111/j.1462-2920.2006.01074.x 1:CAS:528:DC%2BD28XhtFams7fE (Pubitemid 44326477)
80. JS Sinninghe Damste M Strous WI Rijpstra EC Hopmans JA Geenevasen AC van Duin LA van Niftrik MS Jetten 2002 Linearly concatenated cyclobutane lipids form a dense bacterial membrane Nature 419 708 712 10.1038/nature01128 1:CAS:528:DC%2BD38XnvVyrt7Y%3D (Pubitemid 35177953)
81. JS Sinninghe Damste WI Rijpstra JA Geenevasen M Strous MS Jetten 2005 Structural identification of ladderane and other membrane lipids of planctomycetes capable of anaerobic ammonium oxidation (anammox) FEBS J 272 4270 4283 10.1111/j.1742-4658.2005.04842.x 1:CAS:528:DC%2BD2MXps1Kqsbo%3D (Pubitemid 41160932)
82. AO Sliekers N Derwort JL Gomez M Strous JG Kuenen MS Jetten 2002 Completely autotrophic nitrogen removal over nitrite in one single reactor Water Res 36 2475 2482 10.1016/S0043-1354(01)00476-6 1:CAS:528:DC%2BD38XktFaqtrs%3D (Pubitemid 34575598)
83. 15N isotope pairing and dilution at four infiltration rates Appl Environ Microbiol 62 2345 2351 1:CAS:528: DyaK28XjvFGntL0%3D (Pubitemid 26231198)
84. M Strous JJ Heijnen JG Kuenen MSM Jetten 1998 The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms Appl Microbiol Biotechnol 50 589 596 10.1007/s002530051340 1:CAS:528:DyaK1cXotVejsb8%3D (Pubitemid 28555299)
85. M Strous JA Fuerst EH Kramer S Logemann G Muyzer KT van de Pas-Schoonen R Webb JG Kuenen MS Jetten 1999 Missing lithotroph identified as new planctomycete Nature 400 446 449 10.1038/22749 1:CAS:528:DyaK1MXltVGnt7c%3D (Pubitemid 29361796)
86. M Strous E Pelletier S Mangenot T Rattei A Lehner MW Taylor M Horn H Daims D Bartol-Mavel P Wincker V Barbe N Fonknechten D Vallenet B Segurens C Schenowitz-Truong C Medigue A Collingro B Snel BE Dutilh HJ Op den Camp C van der Drift I Cirpus KT van de Pas-Schoonen HR Harhangi L van Niftrik M Schmid J Keltjens J van de Vossenberg B Kartal H Meier D Frishman MA Huynen HW Mewes J Weissenbach MS Jetten M Wagner D Le Paslier 2006 Deciphering the evolution and metabolism of an anammox bacterium from a community genome Nature 440 790 794 10.1038/nature04647
87. Y Tal JE Watts HJ Schreier 2005 Anaerobic ammonia-oxidizing bacteria and related activity in Baltimore inner harbor sediment Appl Environ Microbiol 71 1816 1821 10.1128/AEM.71.4.1816-1821.2005 1:CAS:528:DC%2BD2MXjsVOqtL8%3D (Pubitemid 40546098)
88. 2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments Appl Environ Microbiol 68 1312 1318 10.1128/AEM.68.3.1312-1318.2002 1:CAS:528:DC%2BD38XitFSjs7g%3D (Pubitemid 34205371)
89. KA Third AO Sliekers JG Kuenen MS Jetten 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 10.1078/0723-2020-00077 1:CAS:528:DC%2BD38Xit1alurY%3D (Pubitemid 34116719)
90. M Tourna TE Ereitag JI Prosser 2010 Stabke isotope probing analysis of interactions between ammonia oxidizers Appl Environ Microbiol 76 2468 2477 10.1128/AEM.01964-09 1:CAS:528:DC%2BC3cXlsVSlsro%3D
91. M Trimmer JC Nicholls B Deflandre 2003 Anaerobic ammonium oxidation measured in sediments along the Thames estuary, United Kingdom Appl Environ Microbiol 69 6447 6454 10.1128/AEM.69.11.6447-6454.2003 1:CAS:528: DC%2BD3sXptVyksLc%3D (Pubitemid 37420176)
92. M Trimmer JC Nicholls N Morley CA Davies J Aldridge 2005 Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment Appl Environ Microbiol 71 1923 1930 10.1128/AEM.71.4.1923-1930.2005 1:CAS:528:DC%2BD2MXjsVOqtbg%3D (Pubitemid 40546113)
93. Tsushima I, Kindaichi T, Okabe S (2007) Quantification of anaerobic ammonium- oxidizing bacteria in enrichment cultures by real-time PCR. Water Res 41:785-794 (Pubitemid 46136435)
94. AA van de Graaf A Mulder P de Bruijn MS Jetten LA Robertson JG Kuenen 1995 Anaerobic oxidation of ammonium is a biologically mediated process Appl Environ Microbiol 61 1246 1251
95. J van de Vossenberg JE Rattray W Geerts B Kartal L van Niftrik EG van Donselaar JS Sinninghe Damste M Strous MS Jetten 2008 Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production Environ Microbiol 10 3210 3219
96. LA van Niftrik JA Fuerst JS Sinninghe Damste JG Kuenen MS Jetten M Strous 2004 The anammoxosome: an intracytoplasmic compartment in anammox bacteria FEMS Microbiol Lett 233 7 13 10.1016/j.femsle.2004.01.044 (Pubitemid 38388415)
97. M Wagner G Rath R Amann H-P Koops K-H Schleifer 1995 In situ identification of ammonia oxidizing bacteria Syst Appl Microbiol 18 251 264 1:CAS:528:DyaK2MXpsVequrc%3D
98. BB Ward AH Devol JJ Rich BX Chang SE Bulow H Naik A Pratihary A Jayakumar 2009 Denitrification as the dominant nitrogen loss process in the Arabian Sea Nature 461 78 81 10.1038/nature08276 1:CAS:528:DC%2BD1MXhtVygsbzL
99. LM Zhang PR Offre J-H He DT Verhamme GW Nicol JI Prosser 2011 Autotrophic ammonia oxidation by soil thaumarchaea Proc Natl Acad Sci USA 107 17240 17245 10.1073/pnas.1004947107
100. G Zhu MS Jetten P Kuschk KF Ettwig C Yin 2010 Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems Appl Microbiol Biotechnol 86 1043 1055 10.1007/s00253-010-2451-4 1:CAS:528:DC%2BC3cXjvVehsr8%3D
101. K Zwirglmaier 2005 Fluorescence in situ hybridisation (FISH)-the next generation FEMS Microbiol Lett 246 151 158 10.1016/j.femsle.2005.04.015 1:CAS:528:DC%2BD2MXktFGisL8%3D (Pubitemid 40724425)