Anammox Bacterial Diversity in Various Aquatic Ecosystems Based on the Detection of Hydrazine Oxidase Genes (hzoA/hzoB)

Microbial Ecology

Volumn 61, Issue 2, 2011, Pages 264-276

  Hirsch, Matthew D ^a   Long, Zachery T ^a   Song, Bongkeun ^a  

^a UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; HYDRAZINE DERIVATIVE; NITROGEN; OXIDOREDUCTASE; RNA 16S;

ARTICLE; BACTERIAL GENE; BACTERIUM; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; ENZYMOLOGY; GENETICS; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; PHYLOGENY; REGRESSION ANALYSIS;

BACTERIA; BIODIVERSITY; CLONING, MOLECULAR; DNA, BACTERIAL; GENES, BACTERIAL; HYDRAZINES; NITROGEN; OXIDOREDUCTASES; PHYLOGENY; REGRESSION ANALYSIS; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; WATER MICROBIOLOGY;

BACTERIA (MICROORGANISMS); CANDIDATUS JETTENIA; CANDIDATUS SCALINDUA; PLANCTOMYCETES;

EID: 79951511604     PISSN: 00953628     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00248-010-9743-1     Document Type: Article

References (65)

1. Amano T, Yoshinaga I, Okada K, Yamagishi T, Ueda S, Obuchi A, Sako Y, Suwa Y (2007) Detection of anammox activity and diversity of anammox bacteria-related 16S rRNA genes in coastal marine sediment in Japan. Microbes Environ 22: 232-242.
2. Arrigo KR (2005) Marine microorganisms and global nutrient cycles. Nature 437: 349-355.
3. Bernhard AE, Donn T, Giblin AE, Stahl DA (2005) Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environ Microbiol 7: 1289-1297.
4. Bernhard AE, Tucker J, Giblin AE, Stahl DA (2007) Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environ Microbiol 9: 1439-1447.
5. Braker G, Zhou J, Wu L, Devol AH, Tiedje JM (2000) Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in Pacific northwest marine sediment communities. Appl Environ Microbiol 66: 1893-1900.
6. Bulow SE, Francis CA, Jackson GA, Ward BB (2008) Sediment denitrifier community composition and nirS gene expression investigated with functional gene microarrays. Environ Microbiol 10: 3057-3069.
7. Byrne N, Strous M, Crépeau V, Kartal B, Birrien J-L, Schmid M, Lesongeur F, Schouten S, Jaeschke A, Jetten M, Prieur D, Godfroy A (2009) Presence and activity of anaerobic ammonium-oxidizing bacteria at deep sea hydrothermal vents. ISME J 3: 117-123.
8. Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol 11: 1194-1207.
9. Francis CA, Beman JM, Kuypers MMM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J 1: 19-27.
10. Francis CA, O'Mullan GD, Ward BB (2003) Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiol 1: 129-140.
11. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Nat Acad Sci USA 102: 14683-14688.
12. Freitag TE, Chang L, Prosser JI (2006) Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient. Environ Microbiol 8: 684-696.
13. Galán A, Molina V, Thamdrup B, Woebken D, Lavik G, Kuypers MMM, Ulloa O (2009) Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile. Deep Sea Res II 56: 1021-1031.
14. van de Graaf AA, Mulder A, de Bruijn P, Jetten MS, Robertson LA, Kuenen JG (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 61: 1246-1251.
15. Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, Sinninghe Damsté JS, Krüger S, Graco M, Gutiérrez D, Kuypers MMM (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52: 923-933.
16. Hamersley MR, Woebken D, Boehrer B, Schultze M, Lavik G, Kuypers MMM (2009) Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany). Syst Appl Microbiol 32: 571-582.
17. Herfort L, Kim JH, Coolen MJL, Abbas B, Schouten S, Herndl GJ, Damsté JSS (2009) Diversity of archaea and detection of crenarchaeotal amoA genes in the rivers Rhine and Têt. Aquat Microb Ecol 55: 189-201.
18. Hoffman F, Radax R, Woebken D, Holtappels M, Lavik G, Rapp HT, Schläppy M-L, Schleper C, Kuypers MMM (2009) Complex nitrogen cycling in the sponge Geodia barretti. Environ Microbiol 11: 2228-2243.
19. Humbert S, Tarnawski S, Fromin N, Mallet M-P, Aragno M, Zopfi J (2010) Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J 4: 450-454.
20. Jayakumar DA, Francis CA, Naqvi SWA, Ward BB (2004) Diversity of nitrite reductase genes (nirS) in the denitrifying water column of the coastal Arabian Sea. Aquat Microb Ecol 34: 69-78.
21. Kartal B, van Niftrik L, Rattray J, van de Vossenberg JLCM, Schmid MC, Damsté JS, Jetten MSM, Strous M (2008) Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol 63: 46-55.
22. Kartal B, Rattray J, van Niftrik LA, van de Vossenberg J, Schmid MC, Webb RI, Shouten S, Fuerst JA, Sinninghe Damsté J, Jetten MSM, Strous M (2007) Candidatus "Anammoxoglobus propionicus" a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30: 39-49.
23. Kim O-S, Junier P, Imhoff JF, Witzel K-P (2006) Comparative analysis of ammonia-oxidizing bacterial communities in two lakes in North Germany and the Baltic Sea. Arch Hydrobiol 167: 335-350.
24. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111-120.
25. Kirkpatrick J, Oakley B, Fuchsman C, Srinivasan S, Staley JT, Murray JW (2006) Diversity and distribution of Planctomycetes and related bacteria in the suboxic zone of the Black Sea. Appl Environ Microbiol 72: 3079-3083.
26. Klotz MG, Schmid MC, Strous M, op den Camp HJM, Jetten MSM, Hooper AB (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.
27. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55: 485-529.
28. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163.
29. Kuypers MMM, Lavik G, Woebken D, Schmid MC, Fuchs BM, Amann R, Jørgensen BB, Jetten MSM (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci 102: 6478-6483.
30. Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jørgensen BB, Kuenen JG, Sinninghe Damsté J, Strous M, Jetten MSM (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422: 608-611.
31. Li X-R, Du B, Fu H-X, Wang R-F, Shi J-H, Wang Y, Jetten MSM, Quan Z-X (2009) The bacterial diversity in an anaerobic ammonium-oxidizing (anammox) reactor community. Syst Appl Microbiol 32: 278-289.
32. Li M, Hong Y, Klotz MG, Gu J-D (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.
33. Lozupone C, Hamady M, Knight R (2006) UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinform 7: 371.
34. Mincer TJ, Church MJ, Taylor LT, Preston C, Karl DM, DeLong EF (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9: 1162-1175.
35. Oates H, Song B (2008) Molecular detection of dissimilatory arsenate-respiring bacteria in North Carolina groundwater. In: Ahuja S (ed) Arsenic contamination of groundwater: mechanism, analysis, and remediation. Wiley, New York, pp 83-94.
36. O'Mullan GD, Ward BB (2005) Relationship of temporal and spatial variabilities of ammonia-oxidizing bacteria to nitrification rates in Monterey Bay, California. Appl Environ Microbiol 71: 697-705.
37. Penton CR, Devol AH, Tiedje JM (2006) Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl Environ Microbiol 72: 6829-6832.
38. Prieme A, Braker G, Tiedje JM (2002) Diversity of nitrite reductase (nirK and nirS) gene fragments in forested upland and wetland soils. Appl Environ Microbiol 68: 1893-1900.
39. Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops H-P, Wagner M (2000) 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: 5368-5382.
40. Quan Z-X, Rhee S-K, Zuo J-E, Yang Y, Bae J-W, Park JR, Lee S-T, Park Y-H (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10: 3130-3139.
41. Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microbiol Ecol 53: 311-320.
42. Risgaard-Petersen N, Meyer RL, Schmid M, Jetten MSM, Enrich-Prast A, Rysgaard S, Revsbach NP (2004) Anaerobic ammonium oxidation in an estuarine sediment. Aquat Microb Ecol 36: 293-304.
43. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia oxidizing populations. Appl Environ Microbiol 63: 4704-4712.
44. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. J Mol Evol 4: 406-425.
45. Santoro AE, Francis CA, de Sieyes NR, Boehm AB (2008) Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environ Microbiol 10: 1068-1075.
46. Schloss PD, Handelsmann J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501-1506.
47. Schmid MC, Hooper AB, Klotz MG, Woebken D, Lam P, Kuypers MMM, Pommerening-Roeser A, op den Camp HJM, Jetten MSM (2008) Environmental detection of octahaem cytochrome c hydroxylamine/hydrazine oxidoreductase genes of aerobic and anaerobic ammonium-oxidizing bacteria. Environ Microbiol 10: 3140-3149.
48. Schmid MC, Maas B, Dapena A, van de Pas-Schoonen K, van de Vossenberg J, Kartal B, van Niftrik L, Schmidt I, Cirpus I, Kuenen JG, Wagner M, Sinninghe Damsté JS, Kuypers M, Revsbach NP, Mendez R, Jetten MSM, Strous M (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microbiol 71: 1677-1684.
49. Schmid MC, Risgaard-Petersen N, van de Vossenberg J, Kuypers MMM, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D, Dalsgaard T, Rysgaard S, Sejr MK, Strous M, op den Camp HJM, Jetten MSM (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol 9: 1476-1484.
50. Schmid MC, Schmitz-Esser S, Jetten MSM, Wagner M (2001) 16S-23S rDNA intergenic spacer and 23S rDNA of anaerobic ammonium oxidizers: implications for phylogeny and in situ detection. Environ Microbiol 3: 450-459.
51. Schmid MC, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten MSM, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23: 93-106.
52. Schmid MC, Walsh K, Webb R, Rijpstra WI, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Damsté JS, Harris J, Shaw P, Jetten MSM, Strous M (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.
53. Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 10: 1857-1863.
54. Shimamura M, Nishiyama T, Shigetomo H, Toyomoto T, Kawahara Y, Furukawa K, Takao F (2007) Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl Environ Microbiol 73: 1065-1072.
55. Smith CJ, Nedwell DB, Dong LF, Osborn AM (2007) Diversity and abundance of nitrate reductase genes (narG and napA), nitrite reductase genes (nirS and nrfA), and their transcripts in estuarine sediments. Appl Environ Microbiol 73: 3612-3622.
56. Stehr G, Böttcher B, Dittbemer P, Rath G, Koops H-P (1995) The ammonia-oxidizing nitrifying population of the River Elbe estuary. FEMS Microbiol Ecol 17: 177-186.
57. Strous M, Heijen 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 Microbiol Biotechnol 50: 589-596.
58. Strous M, Pelletier E, Magenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Marvel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh BE, op den Camp HJ, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes JW, Weissenbach J, Jetten MSM, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440: 790-794.
59. Taroncher-Oldenburg G, Griner EM, Francis CA, Ward BB (2003) Oligonucleotide microarray for the study of functional gene diversity in the nitrogen cycle in the environment. Appl Environ Microbiol 69: 1159-1171.
60. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk H-P, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic Crenarchaeota in nitrogen cycling. Environ Microbiol 7: 1985-1995.
61. van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Denselaar EG, Sinninghe Damsté JS, Strous M, Jetten MSM (2008) Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol 10: 3120-3129.
62. Ward BB (1995) Diversity of culturable denitrifying bacteria: limits of rDNA RFLP analysis and probes for the functional gene, nitrite reductase. Arch Microbiol 163: 167-175.
63. Webster G, Embley TM, Prosser JI (2002) Grassland management regimens reduce small-scale heterogeneity and species diversity of beta-proteobacterial ammonia oxidizer populations. Appl Environ Microbiol 68: 20-30.
64. Woebken D, Lam P, Kuypers MMM, Naqvi SWA, Kartal B, Strous M, Jetten MSM, Fuchs BM, Amann R (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10: 3106-3119.
65. Yoshie S, Noda N, Tsuneda S, Hirata A, Inamori Y (2004) Salinity decreases nitrate reductase gene diversity in denitrifying bacteria of wastewater treatment systems. Appl Environ Microbiol 70: 3152-3157.