Biodiversity of N-cycle bacteria in nitrogen removing moving bed biofilters for freshwater recirculating aquaculture systems

Aquaculture

Volumn 306, Issue 1-4, 2010, Pages 177-184

  van Kessel, Maartje A H J ^a   Harhangi, Harry R ^a   van de Pas Schoonen, Katinka ^a   van de Vossenberg, Jack ^b   Flik, Gert ^a   Jetten, Mike S M ^a   Klaren, Peter H M ^a   Op den Camp, Huub J M ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b KWR WATERCYCLE RESEARCH INSTITUTE   (Netherlands)

Author keywords

Anammox; Denitrification; Freshwater aquaculture system; Moving bed biofilm reactor; N cycle bacteria; Nitrification

Indexed keywords

AMMONIUM; ANOXIC CONDITIONS; BACTERIUM; BIOASSAY; BIOFILTRATION; BIOREACTOR; DENITRIFICATION; FRESHWATER ENVIRONMENT; GENETIC ANALYSIS; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; NITROGEN CYCLE; OXIDATION; POLLUTANT REMOVAL; RECIRCULATING SYSTEM; SPECIES DIVERSITY; WATER QUALITY;

BACTERIA (MICROORGANISMS); COPROSMA KAUENSIS; CYPRINIDAE; PLANCTOMYCETES;

EID: 77955053329     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2010.05.019     Document Type: Article

References (55)

1. Amann R.I., Binder B.J., Olson R.J., Chisholm S.W., Devereux R., Stahl D.A. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Applied and Environmental Microbiology 1990, 56:1919-1925.
2. Baker G.C., Smith J.J., Cowan D.A. Review and re-analysis of domain-specific 16S primers. Journal of Microbiological Methods 2003, 55:541-555.
3. Brandes J.A., Devol A.H., Deutsch C. New developments in the marine nitrogen cycle. Chemical Reviews 2007, 107:577-589.
4. Brümmer I.H.M., Felske A.D.M., Wagner-Döbler I. Diversity and seasonal changes of uncultured Planctomycetales in river biofilms. Applied and Environmental Microbiology 2004, 70:5049-5101.
5. Crab R., Avnimelech Y., Defoirdt T., Bossier P., Verstraete W. Nitrogen removal techniques in aquaculture for sustainable production. Aquaculture 2007, 270:1-14.
6. Daims H., Brühl A., Amann R., Schleifer K.-H., Wagner M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: Development and evaluation of a more comprehensive probe set. Systematic and Applied Microbiology 1999, 22:434-444.
7. Daims H., Nielsen J.L., Nielsen P.H., Schleifer K.H., Wagner M. In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Applied and Environmental Microbiology 2001, 67:5273-5284.
8. 2 production by the anammox reaction in the anoxic water column of Golfo Culce, Costa Rica. Nature 2003, 422:606-608.
9. Dosdat A., Servais F., Métailler, Huelvan C., Desbruyéres Comparison of nitrogenous losses in five teleost fish species. Aquaculture 1996, 141:107-127.
10. Eding E.H., Kamstra A., Verreth J.A.J., Huisman E.A., Klapwijk A. Design and operation of nitrifying trickling filters in recirculating aquaculture: a review. Aquacultural Engineering 2006, 34:234-260.
11. Egli K., Fanger U., Alvares P.J.J., Siegrist H., van der Meer J., Zehnder A.J.B. Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Archives in Microbiology 2001, 175:198-207.
12. Foesel B.U., Gieseke A., Schwermer C., Stief P., Koch L., Cytryn E., de la Torré J.R., van Rijn J., Minz D., Drake H.L., Schramm A. Nitrosomonas Nm143-like ammonia oxidizers and Nitrospira marina-like nitrite oxidizers dominate the nitrifier community in a marine aquaculture biofilm. FEMS Microbiology Ecology 2008, 63:192-204.
13. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., Oakley B.B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:14683-14688.
14. Gieseke A., Purkhold U., Wagner M., Amann R., Schramm A. Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Applied and Environmental Microbiology 2001, 67:1351-1362.
15. Haaijer S.C.M., van der Welle M.E.W., Schmid M.C., Lamers L.P.M., Jetten M.S.M., Op den Camp H.J.M. Evidence for the involvement of betaproteobacterial Thiobacilli in the nitrate-dependent oxidation of iron sulfide minerals. FEMS Microbiology Ecology 2006, 58:439-448.
16. Hargreaves J.A. Nitrogen biogeochemistry of aquaculture ponds. Aquaculture 1998, 166:181-212.
17. Jetten M.S.M., Wagner M., Fuerst J., van Loosdrecht M., Kuenen G., Strous M. Microbiology and application of the anaerobic ammonium oxidation ('anammox') process. Current Opinion in Biotechnology 2001, 12:283-288.
18. Jetten M.S.M., van Niftrik L., Strous M., Kartal B., Keltjens J.T., Op den Camp H.J.M. Biochemistry and molecular biology of anammox bacteria. Critical Reviews in Biochemistry and Molecular Biology 2009, 44:65-84.
19. Jetten, M.S.M., Op den Camp, H.J.M., Kuenen, J.G., and Strous, M. Description of the family Brocadiales, in: Krieg, N.R., Staley, J.T., Hedlund, B.P., Paster, B.J. Ward, N., Ludwig, W. and Whitman, W.B. (Eds.), Bergey's Manual of Systematic Bacteriology Volume 4, Springer, Heidelberg, Germany, in press.
20. Juretschko S., Timmermann G., Schmid M., Schleifer K.-H., Pommerening-Röser A., Koops K.-H., Wagner M. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Applied and Environmental Microbiology 1998, 64:3042-3051.
21. Kartal B., Koleva M., Arsov R., van der Star W., Jetten M.S.M., Strous M. Adaptation of a freshwater anammox population to high salinity wastewater. Journal of Biotechnology 2006, 126:546-553.
22. Könneke M., Bernhard A.E., de la Torre J.R., Walker C.B., Waterbury J.B., Stahl D.A. Isolation of an autrotrophic ammonia-oxidizing archaeon. Nature 2005, 437:543-546.
23. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics 2008, 9:299-306.
24. Kuypers M.M., Sliekers A.O., Lavik G., Schmid M., Jorgensen B.B., Kuenen J.G., Sinninghe Damste J.S., Strous M., Jetten M.S.M. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 2003, 422:608-611.
25. Kuypers M.M.M., Lavik G., Woebken D., Schmid M., Fuchs B.M., Amann R., Jorgensen B.B., Jetten M.S.M. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:6478-6483.
26. Lahav O., Bar Massada I., Yackoubov D., Zelikson R., Mozes N., Tal Y., Tarre S. Quantification of anammox activity in a denitrification reactor for a recirculating aquaculture system. Aquaculture 2009, 288:76-82.
27. Lam P., Jensen M.M., Lavik G., McGinnis D.F., Müller B., Schubert C.J., Amann R., Thamdrup B., Kuypers M.M.M. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7104-7109.
28. Lam P., Lavik G., Jensen M.M., van de Vossenberg J., Schmid M., Woebken D., Gutiérrez D., Amann R., Jetten M.S.M., Kuypers M.M.M. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:4752-4757.
29. Manz W., Amann R., Ludwig W., Wagner M., Schleifer K.-H. Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Systematic and Applied Microbiology 1992, 15:593-600.
30. Mobarry B.K., Wagner M., Urbain V., Rittmann B.E., Stahl D.A. Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Applied and Environmental Microbiology 1996, 62:2156-2162.
31. Mommsen T.P., Walsh P.J. Biochemical and environmental perspectives on nitrogen metabolism in fishes. Experientia 1992, 48:583-593.
32. Neef A., Amann R., Schlesner H., Schleifer K.-H. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 1998, 144:3257-3266.
33. Pommerening-Roeser A., Rath G., Koops H.-P. Phylogenetic diversity within the genus Nitrosomonas. Systematic and Applied Microbiology 1996, 19:344-351.
34. Rotthauwe J.-H., Witzel K.-P., Liesack W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Applied and Environmental Microbiology 1997, 63:4704-4712.
35. Rusten B., Eikebrokk B., Ulgenes Y., Lygren E. Design and operations of the Kaldnes moving bed biofilm reactors. Aquacultural Engineering 2006, 34:322-331.
36. Sanni S., Forsberg O.I., Bergheim A. A dynamic model for fish metabolite production and water quality in landbased fish farms. Fish Farming Technology 1993, 367-374. A.A. Balkema, Rotterdam. H. Reinertsen, L.A. Dahle, L. Jørgensen, K. Tvinnereim (Eds.).
37. Schmid M., Twachtmann U., Klein M., Strous M., Juretschko S., Jetten M.S.M., Metzger J.W., Schleifer K.H., Wagner M. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Systematic and Applied Microbiology 2000, 23:93-106.
38. Schmid M., Walsh K., Webb R., Rijpstra I.C.W., van de Pas-Schoonen K., Verbruggen J.M., Hill T., Moffet B., Fuerst J., Schouten S., Sinninghe Damstè S.J., Harris J., Shaw P., Jetten M.S.M., Strous M. Two new species of anareobic ammonium oxidizing bacteria. Systematic and Applied Microbiology 2003, 26:529-538.
39. Schmid M.C., Risgaard-Petersen N., van de Vossenberg J., Kuypers M.M.M., Lavik G., Petersen J., Hulth S., Thamdrup B., Canfield D., Dalsgaard T., Rysgaard S., Sejr M.K., Strous M., Op den Camp H.J.M., Jetten M.S.M. Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environmental Microbiology 2007, 9:1476-1484.
40. Schubert C.J., Durisch-Kaiser E., Wehrli B., Thamdrup B., Lam P., Kuypers M.M.M. Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environmental Microbiology 2006, 8:1857-1863.
41. Sliekers A.O., Haaijer S., Schmid M., Harhangi H., Verwegen K., Kuenen J.G., Jetten M.S.M. Nitrification and anammox with urea as the energy source. Systematic and Applied Microbiology 2004, 27:271-278.
42. Stahl D.A., Amann R. Development and application of nucleic acid probes. Nucleic acid techniques in bacterial systematics 1991, 205-248. John Wiley & Sons Ltd., Chichester, England. E. Stackebrandt, M. Goodfellow (Eds.).
43. 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 organisms. Applied Microbiology and Biotechnology 1998, 50:589-596.
44. Tal Y., Watts J.E.M., Schreier S.B., Sowers K.R., Schreier H.J. Characterization of the microbial community and nitrogen transformation process associated with moving bed bioreactors in a closed recirculated mariculture system. Aquaculture 2003, 215:187-202.
45. Tal Y., Watts J.E.M., Schreier H.J. Anaerobic ammonium-oxidizing (anammox) bacteria and associated activity in fixed-film biofilters of a marine recirculating aquaculture system. Applied and Environmental Microbiology 2006, 72:2896-2904.
46. 2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Applied and Environmental Microbiology 2002, 68:1312-1318.
47. Trimmer M., Nicholls J.C., Deflandre B. Anaerobic ammonium oxidation measured in sediments along the Thamees estuary, United Kingdom. Applied and Environmental Microbiology 2003, 69:6447-6454.
48. Trimmer M., Nicholls J.C., Morley N., Davies C.A., Aldridge J. Biphasic behavior of anammox regulated by nitrite and nitrate in an estuarine sediment. Applied and Environmental Microbiology 2005, 71:1923-1930.
49. Van Rijn J. The potential of integrated biological treatment systems in recirculating fish culture-a review. Aquaculture 1996, 139:181-201.
50. Van Rijn J., Tal Y., Schreier H.J. Denitrification in recirculating systems: theory and applications. Aquacultural Engineering 2006, 34:364-376.
51. Wagner M., Rath G., Amann R., Koops H.-P., Schleifer K.-H. In situ identification of ammonia-oxidizing bacteria. Systematic and Applied Microbiology 1995, 18:251-264.
52. Wagner M., Rath G., Koops H.P., Flood J., Amann R. In situ analysis of nitrifying bacteria in sewage treatment plants. Water Science and Technology 1996, 34:237-244.
53. Wang J., Jenkins C., Webb R.I., Fuerst J.A. Isolation of Gemmata-like and Isophaera-like planctomycete bacteria from soil and freshwater. Applied and Environmental Microbiology 2002, 68:417-422.
54. Wilkie M.P. Mechanisms of ammonia excretion across fish gills. Comparative Biochemistry and Physiology 1997, 118A:39-50.
55. Zheng D.D., Alm E.W., Stahl D.A., Raskin L. Characterization of universal small-subunit rRNA hybridization probes for quantitative molecular microbial ecology studies. Applied and Environmental Microbiology 1996, 62:4504-4513.