Mimicking the oxygen minimum zones: Stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system

Environmental Microbiology

Volumn 14, Issue 12, 2012, Pages 3146-3158

  Yan, Jia ^a,b   Haaijer, Suzanne C M ^a   Op den Camp, Huub J M ^a   van Niftrik, Laura ^a   Stahl, David A ^c   Könneke, Martin ^d   Rush, Darci ^e   Sinninghe Damsté, Jaap S ^e   Hu, Yong Y ^b   Jetten, Mike S M ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^c University of Washington   (United States)

^d UNIVERSITY OF BREMEN   (Germany)

^e ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; OXYGEN;

ANAEROBIC BACTERIUM; AQUATIC SPECIES; ARCHAEON; ARTICLE; BETAPROTEOBACTERIA; BIOLOGICAL MODEL; BIOREACTOR; GENETICS; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; OXYGEN CONSUMPTION; PARASITOLOGY; PHYLOGENY; SYMBIOSIS; ULTRASTRUCTURE; WASTE WATER;

AMMONIA; AQUATIC ORGANISMS; ARCHAEA; BACTERIA, ANAEROBIC; BETAPROTEOBACTERIA; BIOREACTORS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXYGEN; OXYGEN CONSUMPTION; PHYLOGENY; SYMBIOSIS; WASTE WATER;

ARCHAEA; BACTERIA (MICROORGANISMS); CANDIDATUS NITROSOPUMILUS MARITIMUS; CANDIDATUS SCALINDUA; NITROSOMONADALES;

EID: 84870493927     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02894.x     Document Type: Article

References (61)

1. Akaike, T., and Maeda, H. (1996) Quantitation of nitric oxide using 2-phenyl-4, 4, 5, 5-tetramethylimidazoline-1-oxyl 3-oxide (PTIO). Methods Enzymol 268: 211-221.
2. Amano, F., and Noda, T. (1995) Improved detection of nitric-oxide radical (NO-center-dot) production in an activated macrophage culture with a radical scavenger, carboxy PTIO, and Griess reagent. FEBS Lett 368: 425-428.
3. Arrigo, K.R. (2005) Marine microorganisms and global nutrient cycles. Nature 437: 349-355.
4. Bagchi, S., Biswas, R., and Nandy, T. (2010) Alkalinity and dissolved oxygen as controlling parameters for ammonia removal through partial nitritation and ANAMMOX in a single-stage bioreactor. J Ind Microbiol Biotechnol 37: 871-876.
5. Beman, J.M., Popp, B.N., and Francis, C.A. (2008) Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME J 2: 429-441.
6. Bernhard, A.E., Landry, Z.C., Blevins, A., de la Torre, J.R., Giblin, A.E., and Stahl, D.A. (2010) Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relation to potential nitrification rates. Appl Environ Microbiol 76: 1285-1289.
7. Bligh, E.G., and Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
8. Coolen, M.J.L., Abbas, B., van Bleijswijk, J., Hopmans, E.C., Kuypers, M.M.M., Wakeham, S.G., etal. (2007) Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids. Environ Microbiol 9: 1001-1016.
9. Ellis, A., Lu, H., Li, C.G., and Rand, M.J. (2001) Effects of agents that inactivate free radical NO (NO center dot) on nitroxyl anion-mediated relaxations, and on the detection of NO center dot released from the nitroxyl anion donor Angeli's salt. Br J Pharmacol 134: 521-528.
10. Francis, C.A., Roberts, K.J., Beman, J.M., Santoro, A.E., and Oakley, B.B. (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102: 14683-14688.
11. Galán, A., Molina, V., Thamdrup, B., Woebken, D., Lavik, G., Kuypers, M.M.M., etal. (2009) Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile. Deep Sea Res Part II Top Stud Oceanogr 56: 1125-1135.
12. van de Graaf, A.A., de Bruijn, P., Robertson, L.A., Jetten, M.S.M., and Kuenen, J.G. (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142: 2187-2196.
13. Hamersley, M.R., Lavik, G., Woebken, D., Rattray, J.E., Lam, P., Hopmans, E.C., etal. (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52: 923-933.
14. Hopmans, E.C., Kienhuis, M.V.M., Rattray, J.E., Jaeschke, A., Schouten, S., and Sinninghe Damsté, J.S. (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.
15. Jaeschke, A., Hopmans, E.C., Wakeham, S.G., Schouten, S., and Sinninghe Damsté, J.S. (2007) The presence of ladderane lipids in the oxygen minimum zone of the Arabian Sea indicates nitrogen loss through anammox. Limnol Oceanogr 82: 780-786.
16. Jaeschke, A., Op den Camp, H.J.M., Harhangi, H., Klimiuk, A., Hopmans, E.C., Jetten, M.S.M., etal. (2009) 16S rRNA gene and lipid biomarker evidence for anaerobic ammonium-oxidizing bacteria (anammox) in California and Nevada hot springs. FEMS Microbiol Ecol 67: 343-350.
17. Jaeschke, A., Abbas, B., Zabel, M., Hopmans, E.C., Schouten, S., and Sinninghe Damsté, J.S. (2010) Molecular evidence for anaerobic ammonium-oxidizing (anammox) bacteria in continental shelf and slope sediments off northwest Africa. Limnol Oceanogr 55: 365-376.
18. Jensen, M.M., Lam, P., Revsbech, N.P., Nagel, B., Gaye, B., Jetten, M.S.M., and Kuypers, M.M.M. (2011) Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J 5: 1660-1670.
19. Jetten, M.S.M. (2008) The microbial nitrogen cycle. Environ Microbiol 10: 2903-2909.
20. Jia, Z.J., and Conrad, R. (2009) Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11: 1658-1671.
21. Kartal, B., Kuenen, J.G., and van Loosdrecht, M.C.M. (2010) Sewage treatment with anammox. Science 328: 702-703.
22. Könneke, M., Bernhard, A.E., Torre, J.R., Walker, C.B., Waterbury, J.B., and Stahl, D.A. (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437: 543-546.
23. Kuypers, M.M.M., Sliekers, A.O., Lavik, G., Schmid, M., Jorgensen, B.B., Kuenen, J.G., etal. (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422: 608-611.
24. Kuypers, M.M.M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B.M., Amann, R., etal. (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA 102: 6478-6483.
25. Lam, P., and Kuypers, M.M.M. (2011) Microbial nitrogen cycling processes in oxygen minimum zones. Ann Rev Mar Sci 3: 317-345.
26. Lam, P., Jensen, M.M., Lavik, G., McGinnis, D.F., Muller, B., Schubert, C.J., etal. (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 104: 7104-7109.
27. Lam, P., Lavik, G., Jensen, M.M., van de Vossenberg, J., Schmid, M., Woebken, D., etal. (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106: 4752-4757.
28. Martens-Habbena, W., Berube, P.M., Urakawa, H., de la Torre, H.J.R., and Stahl, D.A. (2009) Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461: 976-978.
29. Mincer, T.J., Church, M.J., Taylor, L.T., Preston, C., Kar, D.M., and DeLong, E.F. (2007) Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre. Environ Microbiol 9: 1162-1175.
30. Mulder, A., van de Graaf, A.A., Robertson, L.A., and Kuenen, J.G. (1995) Anaerobic ammonium oxidation discovered in denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16: 177-183.
31. van Niftrik, L.A., Fuerst, J.A., Damste, J.S.S., Kuenen, J.G., Jetten, M.S.M., and Strous, M. (2004) The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 233: 7-13.
32. van Niftrik, L., Geerts, W.J.C., van Donselaar, E.G., Humbel, B.M., Webb, R.I., Fuerst, J.A., etal. (2008a) Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome c proteins. J Bacteriol 190: 708-717.
33. van Niftrik, L., Geerts, W.J.C., van Donselaar, E.G., Humbel, B.M., Yakushevska, A., Verkleij, A.J., etal. (2008b) Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J Struct Biol 161: 401-410.
34. Parker, C.T., Huynh, S., Quinones, B., Harris, L.J., and Mandrell, R.E. (2010) Comparison of genotypes of Salmonella enterica serovar enteritidis phage type 30 and 9c strains isolated during three outbreaks associated with raw almonds. Appl Environ Microbiol 76: 3723-3731.
35. Paulmier, A., and Ruiz-Pino, D. (2009) Oxygen minimum zones (OMZs) in the modern ocean. Prog Oceanogr 80: 113-128.
36. Pitcher, A., Villanueva, L., Hopmans, E.C., Schouten, S., Reichart, G.J., and Sinninghe Damsté, J.S. (2011) Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. ISME J 5: 1896-1904.
37. Rattray, J.E., van de Vossenberg, J., Hopmans, E.C., Kartal, B., van Niftrik, L., Rijpstra, W.I.C., etal. (2008) Ladderane lipid distribution in four genera of anammox bacteria. Arch Microbiol 190: 51-66.
38. Rusch, A., Hannides, A.K., and Gaidos, E. (2009) Diverse communities of active Bacteria and Archaea along oxygen gradients in coral reef sediments. Coral Reefs 28: 15-26.
39. Rush, D., Hopmans, E.C., Wakeham, S.G., Schouten, S., and Sinninghe Damsté, J.S. (2012a) Occurrence and distribution of ladderane oxidation products in different oceanic regimes. Biogeosciences 9: 2407-2418.
40. Rush, D., Wakeham, S.G., Hopmans, E.C., Schouten, S., and Sinninghe Damsté, J.S. (2012b) Biomarker evidence for anammox in the oxygen minimum zone of the Eastern Tropical North Pacific. Org Geochem doi: 10.1016/j.orggeochem.2012.02.005.
41. Schmid, M.C., Risgaard-Petersen, N., van de Vossenberg, J., Kuypers, M.M.M., Lavik, G., Petersen, J., etal. (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol 9: 1476-1484.
42. Schouten, S., van der Meer, M.T.J., Hopmans, E.C., Rijpstra, W.I.C., Reysenbach, A.L., Ward, D.M., etal. (2007) Archaeal and bacterial glycerol dialkyl glycerol tetraether lipids in hot springs of Yellowstone National Park. Appl Environ Microbiol 73: 6181-6191.
43. Sinninghe Damsté, J.S., Rijpstra, W.I.C., Hopmans, E.C., Prahl, F.G., Wakeham, S.G., and Schouten, S. (2002a) Distribution of membrane lipids of planktonic Crenarchaeota in the Arabian Sea. Appl Environ Microbiol 68: 2997-3002.
44. Sinninghe Damsté, J.S., Schouten, S., Hopmans, E.C., van Duin, A.C.T., and Geenevasen, J.A.J. (2002b) Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J Lipid Res 43: 1641-1651.
45. Sinninghe Damsté, J.S., Strous, M., Rijpstra, W.I.C., Hopmans, E.C., Geenevasen, J.A.J., van Duin, A.C.T., etal. (2002c) Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419: 708-712.
46. Sliekers, A.O., Derwort, N., Gomez, J.L.C., Strous, M., Kuenen, J.G., and Jetten, M.S.M. (2002) Completely autotrophic nitrogen removal over nitrite in one single reactor. Water Res 36: 2475-2482.
47. Stewart, F.J., Ulloa, O., and DeLong, E.F. (2012) Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol 14: 23-40.
48. Strous, M., van Gerven, E., Kuenen, J.G., and Jetten, M. (1997) Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (Anammox) sludge. Appl Environ Microbiol 63: 2446-2448.
49. Taylor, S., Ninjoor, V., Dowd, D.M., and Tappel, A.L. (1974) Cathepsin B2 measurement by sensitive fluorometric ammonia analysis. Anal Biochem 60: 153-162.
50. Vázquez-Padín, J.R., Pozo, M.J., Jarpa, M., Figueroa, M., Franco, A., Mosquera-Corral, A., etal. (2009) Treatment of anaerobic sludge digester effluents by the CANON process in an air pulsing SBR. J Hazard Mater 166: 336-341.
51. Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., etal. (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74.
52. Verhamme, D.T., Prosser, J.I., and Nicol, G.W. (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5: 1067-1071.
53. van de Vossenberg, J., Rattray, J.E., Geerts, W., Kartal, B., van Niftrik, L., van Donselaar, E.G., etal. (2008) Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol 10: 3120-3129.
54. van de Vossenberg, J., Woebken, D., Maalcke, W.J., Wessels, H.J.C.T., Dutilh, B.E., Kartal, B., etal. (2012) The metagenome of the marine anammox bacterium 'Candidatus Scalindua profunda' illustrates the versatility of this globally important nitrogen cycle bacterium. Environ Microbiol doi: 10.1111/j.1462-2920.2012.02774.x.
55. Wakeham, S.G., Turich, C., Schubotz, F., Podlaska, A., Li, X.N., Varela, R., etal. (2012) Biomarkers, chemistry and microbiology show chemoautotrophy in a multilayer chemocline in the Cariaco Basin. Deep Sea Res Part I Oceanogr Res Pap 63: 133-156.
56. Walker, C.B., de la Torre, J.R., Klotz, M.G., Urakawa, H., Pinel, N., Arp, D.J., etal. (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107: 8818-8823.
57. Woebken, D., Fuchs, B.A., Kuypers, M.A.A., and 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.
58. Woebken, D., Lam, P., Kuypers, M.M.M., Naqvi, S.W.A., Kartal, B., Strous, M., etal. (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10: 3106-3119.
59. Wuchter, C., Abbas, B., Coolen, M.J.L., Herfort, L., van Bleijswijk, J., Timmers, P., etal. (2006) Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 103: 12317-12322.
60. Yan, J., Op den Camp, H.J.M., Jetten, M.S.M., Hu, Y.Y., and Haaijer, S.C.M. (2010) Induced cooperation between marine nitrifiers and anaerobic ammonium-oxidizing bacteria by incremental exposure to oxygen. Syst Appl Microbiol 33: 407-415.
61. 2 addition to an AUSB reactor. J Chem Technol Biotechnol 85: 204-208.