Evaluating Primers for Profiling Anaerobic Ammonia Oxidizing Bacteria within Freshwater Environments

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Sonthiphand, Puntipar ^a   Neufeld, Josh D ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GROUND WATER; RNA 16S;

AMMONIA OXIDIZING BACTERIUM; AMPLICON; ARTICLE; BACTERIUM DETECTION; CANDIDATUS BROCADIA; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA FINGERPRINTING; DNA MODIFICATION; FRESHWATER ENVIRONMENT; GC CLAMP MODIFICATION; GENE CLUSTER; GENE IDENTIFICATION; GENETIC ANALYSIS; INTERMETHOD COMPARISON; LAKE SEDIMENT; MICROBIAL DIVERSITY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; VALIDATION PROCESS;

AMMONIA; BACTERIA, ANAEROBIC; BIODIVERSITY; DNA PRIMERS; DNA, BACTERIAL; ECOSYSTEM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FRESH WATER; GENE EXPRESSION PROFILING; MOLECULAR SEQUENCE DATA; ONTARIO; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S;

EID: 84874706783     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057242     Document Type: Article

References (64)

1. Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, et al. (1999) Missing lithotroph identified as new planctomycete. Nature 400: 446-449.
2. Schmid MC, Maas B, Dapena A, van de Pas-Schoonen K, van de Vossenberg J, et al. (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microbiol 71: 1677-1684.
3. Jetten MSM, Sliekers O, Kuypers MMM, Dalsgaard T, van Niftrik L, et al. (2003) Anaerobic ammonium oxidation by marine and freshwater planctomycete-like bacteria. Appl Microbiol Biotechnol 63: 107-114.
4. Broda E, (1977) Two kinds of lithotrophs missing in nature. Z Allg Mikrobiol 17: 491-493.
5. Richards FA (1965) Anoxic basins and fjords. In: Ripley JP, Skirrow G, editors. Chemical Oceanography. pp. 611-645.
6. Helmer C, Kunst S, Juretschko S, Schmid MC, Schleifer KH, et al. (1999) Nitrogen loss in a nitrifying biofilm system. Water Sci Technol 39: 13-21.
7. Mulder A, van de Graaf AA, Robertson LA, Kuenen JG, (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol 16: 177-183.
8. Li M, Hong Y, Klotz MG, Gu JD, (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.
9. Dang H, Chen R, Wang L, Guo L, Chen P, et al. (2010) Environmental factors shape sediment anammox bacterial communities in hypernutrified Jiaozhou Bay, China. Appl Environ Microbiol 76: 7036-7047.
10. Hong YG, Yin B, Zheng TL, (2011) Diversity and abundance of anammox bacterial community in the deep-ocean surface sediment from equatorial Pacific. Appl Microbiol Biotechnol 89: 1233-1241.
11. 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: 264-276.
12. Mohamed NM, Saito K, Tal Y, Hill RT, (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4: 38-48.
13. Thamdrup B, Dalsgaard T, (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68: 1312-1318.
14. Engstrom P, Penton CR, Devol AH, (2009) Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol Oceanogr 54: 1643-1652.
15. Brandsma J, van de Vossenberg J, Risgaard-Petersen N, Schmid MC, Engström P, et al. (2011) A multi-proxy study of anaerobic ammonium oxidation in marine sediments of the Gullmar Fjord, Sweden. Environ Microbiol Rep 3: 360-366.
16. Trimmer M, Nicholls JC, (2009) 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: 577-589.
17. Moore TA, Xing Y, Lazenby B, Lynch MD, Schiff S, et al. (2011) Prevalence of anaerobic ammonium-oxidizing bacteria in contaminated groundwater. Environ Sci Technol 45: 7217-7225.
18. Zhu G, Wang S, Wang Y, Wang C, Risgaard-Petersen N, et al. (2011) Anaerobic ammonia oxidation in a fertilized paddy soil. ISME J 5: 1905-1912.
19. Strous M, Heijnen 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.
20. Manz W, Amann RI, Ludwig W, Wagner M, Schleifer KH, (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593-600.
21. Schmid MC, Schmitz-Esser S, Jetten MSM, Wagner M, (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.
22. 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.
23. 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.
24. Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, et al. (2010) Molecular detection of anammox bacteria in terrestrial ecosystems: distribution and diversity. ISME J 4: 450-454.
25. Schmid MC, Twachtmann U, Klein M, Strous M, Juretschko S, et al. (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23: 93-106.
26. Schmid MC, Walsh K, Webb R, Rijpstra WI, van de Pas-Schoonen K, et al. (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.
27. Amano T, Yoshinaga I, Okada K, Yamagishi T, Ueda S, et al. (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.
28. Rich JJ, Dale OR, Song B, Ward BB, (2008) Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microb Ecol 55: 311-320.
29. Zhang Y, Ruan XH, Op den Camp HJM, Smits TJM, Jetten MSM, et al. (2007) Diversity and abundance of aerobic and anaerobic ammonium-oxidizing bacteria in freshwater sediments of the Xinyi River (China). Environ Microbiol 9: 2375-2382.
30. Tal Y, Watts JEM, Schreier HJ, (2005) Anaerobic ammonia-oxidizing bacteria and related activity in Baltimore inner harbor sediment. Appl Environ Microbiol 71: 1816-1821.
31. Tal Y, Watts JEM, Schreier HJ, (2006) Anaerobic ammonium-oxidizing (anammox) bacteria and associated activity in fixed-film biofilters of a marine recirculating aquaculture system. Appl Environ Microbiol 72: 2896-2904.
32. Kirkpatrick J, Oakley B, Fuchsman C, Srinivasan S, Staley JT, et al. (2006) Diversity and distribution of Planctomycetes and related bacteria in the suboxic zone of the Black Sea. Appl Environ Microbiol 72: 3079-3083.
33. Kuypers MMM, Sliekers AO, Lavik G, Schmid MC, Jørgensen BB, et al. (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422: 608-611.
34. Dalsgaard T, Thamdrup B, Canfield DE, (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156: 457-464.
35. Schubert CJ, Durisch-Kaiser E, Wehrli B, Lam P, Kuypers MMM, (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 8: 1857-1863.
36. Yoshinaga I, Amano T, Yamagishi T, Okada K, Ueda S, et al. (2011) Distribution and diversity of anaerobic ammonium oxidation (anammox) bacteria in the sediment of a eutrophic freshwater lake, Lake Kitaura, Japan. Microbes Environ 26: 189-197.
37. Humbert S, Zopfi J, Tarnawski SE, (2012) Abundance of anammox bacteria in different wetland soils. Environ Microbiol Rep 4: 484-490.
38. Zhu G, Wang S, Feng X, Fan G, Jetten MSM, et al. (2011) Anammox bacterial abundance, biodiversity and activity in a constructed wetland. Environ Sci Technol 45: 9951-9958.
39. Hu BL, Rush D, van der Biezen E, Zheng P, van Mullekom M, et al. (2011) New anaerobic, ammonium-oxidizing community enriched from peat soil. Appl Environ Microbiol 77: 966-971.
40. Hu B, Shen L, Du P, Zheng P, Xu X, et al. (2012) The influence of intense chemical pollution on the community composition, diversity and abundance of anammox bacteria in the Jiaojiang Estuary (China). PloS ONE 7: e33826.
41. Hong YG, Li M, Cao H, Gu JD, (2011) Residence of habitat-specific anammox bacteria in the deep-sea subsurface sediments of the South China Sea: analyses of marker gene abundance with physical chemical parameters. Microb Ecol 62: 36-47.
42. Li H, Chen S, Mu BZ, Gu JD, (2010) Molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in high-temperature petroleum reservoirs. Microb Ecol 60: 771-783.
43. Woebken D, Fuchs BM, Kuypers MMM, Amann R, (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73: 4648-4657.
44. van der Star WRL, Miclea AI, van Dongen UGJM, Muyzer G, Picioreanu C, et al. (2008) The membrane bioreactor: A novel tool to grow anammox bacteria as free cells. Biotechnol Bioeng 101: 286-294.
45. Bae H, Park KS, Chung YC, Jung JY, (2010) Distribution of anammox bacteria in domestic WWTPs and their enrichments evaluated by real-time quantitative PCR. Process Biochem 45: 323-334.
46. Neufeld JD, Schafer H, Cox MJ, Boden R, McDonald IR, et al. (2007) Stable-isotope probing implicates Methylophaga spp. and novel Gammaproteobacteria in marine methanol and methylamine metabolism. ISME J 1: 480-491.
47. Green SJ, Leigh MB, Neufeld JD (2010) Denaturing gradient gel electrophoresis (DGGE) for microbial community analysis. In: Timmis K, editor. Hydrocarbon Microbiology. Berlin: Springer. pp. 4137-4158.
48. Lynch MDJ, Masella AP, Hall MW, Bartram AK, Neufeld JD, (2013) AXIOME: automated exploration of microbial diversity. Gigascience In press.
49. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32: 1792-1797.
50. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum composite likelihood. Syst Biol 52: 696-704.
51. Galtier N, Gouy M, Gautier C, (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogenies. Bioinformatics 12: 543-548.
52. Sonthiphand P, Cejudo E, Schiff S, Neufeld JD, (2012) Microbiology of ammonia oxidation in the Grand River: disentangling molecular signatures of wastewater effluent from autochthonous prokaryotic communities. Environ Microbiol (submitted).
53. Lam P, Jensen MM, Lavik G, McGinnis DF, Muller B, et al. (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 104: 7104-7109.
54. Schmid MC, Risgaard-Petersen N, van de Vossenberg J, Kuypers MMM, Lavik G, et al. (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol 9: 1476-1484.
55. Ward BB, Devol AH, Rich JJ, Chang BX, Bulow SE, et al. (2009) Denitrification as the dominant nitrogen loss process in the Arabian Sea. Nature 461: 78-81.
56. Woebken D, Lam P, Kuypers MMM, Naqvi SW, Kartal B, et al. (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10: 3106-3119.
57. Hamersley MR, Woebken D, Boehrer B, Schultze M, Lavik G, et al. (2009) Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany). Syst Appl Microbiol 32: 571-582.
58. Li M, Hong YG, Cao HL, Gu JD, (2011) Mangrove trees affect the community structure and distribution of anammox bacteria at an anthropogenic-polluted mangrove in the Pearl River Delta reflected by 16S rRNA and hydrazine oxidoreductase (HZO) encoding gene analyses. Ecotoxicology 20: 1780-1790.
59. Li M, Ford T, Li XY, Gu JD, (2011) Cytochrome cd1-containing nitrite encoding gene nirS as a new functional biomarker for detection of anaerobic ammonium oxidizing (Anammox) bacteria. Envion Sci Technol 45: 3547-3553.
60. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid MC, et al. (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106: 4752-4757.
61. Harhangi HR, Roy ML, van Alen T, Hu BL, Groen J, et al. (2012) Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria. Appl Environ Microbiol 78: 752-758.
62. Neef A, Arnann R, Schlesner H, Schleiferl KH, (1998) Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 144: 3257-3266.
63. Ferris M, Muyzer G, Ward D, (1996) Denaturing gradient gel electrophoresis profiles of 16S rRNA-defined populations inhabiting a hot spring microbial mat community. Appl Environ Microbiol 62: 340-346.
64. Muyzer G, de Waal EC, Uitterlinden AG, (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S ribosomal RNA. Appl Environ Microbiol 59: 695-700.