Estuarine nitrifiers: New players, patterns and processes

Estuarine, Coastal and Shelf Science

Volumn 88, Issue 1, 2010, Pages 1-11

  Bernhard, Anne E ^a   Bollmann, Annette ^b  

^a The Holleran Center for Community Action and Public Policy   (United States)

^b MIAMI UNIVERSITY   (United States)

Author keywords

ammonia oxidizing archaea; ammonia oxidizing bacteria; amoA; Estuary; Nitrosopumilus maritimus; salt marsh

Indexed keywords

ABUNDANCE; AMMONIA; ESTUARINE ECOSYSTEM; NICHE PARTITIONING; OXIC CONDITIONS; OXIDATION; PARADIGM SHIFT; PHYLOGENETICS; PHYSICOCHEMICAL PROPERTY; PROKARYOTE; SALINITY; SALTMARSH;

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

EID: 77953138654     PISSN: 02727714     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecss.2010.01.023     Document Type: Article

References (97)

1. Acinas S.G., Sarma-Rupavtarm R., Klepac-Ceraj V., and Polz M.F. PCR-induced sequence artifacts and bias: insights from comparison of two 16S rRNA clone libraries constructed from the same sample. Applied and Environmental Microbiology 71 (2005) 8966-8969
2. Agogue H., Brink M., Dinasquet J., and Herndl G.J. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic. Nature 456 (2008) 788-792
3. Alzerreca J.J., Norton J.M., and Klotz M.G. The amo operon in marine, ammonia-oxidizing gammaproteobacteria. FEMS Microbiology Letters 180 (1999) 21-29
4. Amann R.I., Ludwig W., and Schleifer K.-H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiological Reviews 59 (1995) 143-169
5. An S., and Joye S.B. Enhancement of coupled nitrification-denitrification by benthic photosynthesis in shallow estuarine sediments. Limnology and Oceanography 46 (2001) 62-74
6. Anderson I.C., Tobias C.R., Neikirk B.B., and Wetzel R.L. Development of a process-based nitrogen mass balance model for a Virginia (USA) Spartina alterniflora salt marsh: implications for net DIN flux. Marine Ecology Progress Series 159 (1997) 13-27
7. Beman J.M., Roberts K.J., Wegley L., Rohwer F., and Francis C.A. Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Applied and Environmental Microbiology 73 (2007) 5642-5647
8. Beman J.M., Popp B.N., and Francis C.A. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California. ISME Journal 2 (2008) 429-441
9. Beman J.M., and Francis C.A. Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahi'a del To'bari, Mexico. Applied and Environmental Microbiology 72 (2006) 7767-7777
10. Bernhard A.E., Colbert D., McManus J., and Field K.G. Microbial community dynamics based on 16S rRNA gene profiles in a Pacific Northwest estuary and its tributaries. FEMS Microbiology Ecology 52 (2005) 115-128
11. Bernhard A.E., Donn T., Giblin A.E., and Stahl D.A. Loss of diversity of ammonia-oxidizing bacteria correlates with increasing salinity in an estuary system. Environmental Microbiology 7 (2005) 1289-1297
12. Bernhard A.E., Tucker J., Giblin A.E., and Stahl D.A. Functionally distinct communities of ammonia-oxidizing bacteria along an estuarine salinity gradient. Environmental Microbiology 9 (2007) 1439-1447
13. Bernhard A.E., Landry Z.C., Blevins A., de la Torre J.R., Giblin A.E., and Stahl D.A. Abundance of ammonia-oxidizing archaea and bacteria along an estuarine salinity gradient in relationship to potential nitrification rates. Applied and Environmental Microbiology 76 (2010) 1284-1289
14. Dang H., Zhang X., Sun J., Tiegang L., Zhang Z., and Yang G. Diversity and spatial distribution of sediment ammonia-oxidizing crenarchaeota in response to estuarine and environmental gradients in the Changjiang Estuary and East China Sea. Microbiology 154 (2008) 2084-2095
15. de Bie M.J.M., Speksnijder A., Kowalchuk G.A., Schuurman T., Zwart G., Stephen J.R., Diekmann O.E., and Laanbroek H.J. Shifts in the dominant populations of ammonia-oxidizing beta-subclass proteobacteria along the eutrophic Schelde estuary. Aquatic Microbial Ecology 23 (2001) 225-236
16. de La Torre J.R., Walker C.B., Ingalls A.E., Könneke M., and Stahl D.A. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environmental Microbiology 10 (2008) 810-818
17. del Giorgio, P.A., Bouvier, T.C, 2002. Linking the physiologic and phylogenetic successions in free-living bacterial communities along an estuarine salinity gradient. 47, 471-486.
18. Bintrim S.B., Donohue T.J., Handelsman J., Roberts G.P., and Goodman R.M. Molecular phylogeny of Archaea from soil. Proceedings of the National Academy of Sciences of the United States of America 94 (1997) 277-282
19. + adsorption in marine-sediments - process and controls of adsorption. Limnology and Oceanography 27 (1982) 99-110
20. Bodelier P.L.E., Libochant J.A., Blom C., and Laanbroek H.J. Dynamics of nitrification and denitrification in root-oxygenated sediments and adaptation of ammonia-oxidizing bacteria to low-oxygen or anoxic habitats. Applied and Environmental Microbiology 62 (1996) 4100-4107
21. Bollmann A., Bar-Gilissen M.J., and Laanbroek H.J. Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Applied and Environmental Microbiology 68 (2002) 4751-4757
22. Bollmann A., and Laanbroek H.J. Influence of oxygen partial pressure and salinity on the community composition of ammonia-oxidizing bacteria in the Schelde estuary. Aquatic Microbial Ecology 28 (2002) 239-247
23. Boynton W.R., and Kemp W.M. Nutrient regeneration and oxygen-consumption by sediments along an estuarine salinity gradient. Marine Ecology Progress Series 23 (1985) 45-55
24. Caffrey J.M., Bano N., Kalanetra K., and Hollibaugh J.T. Ammonia oxidation and ammonia-oxidizing bacteria and archaea from estuaries with differing histories of hypoxia. ISME Journal 1 (2007) 660-662
25. Chen X.-P., Zhu Y.-G., Xia Y., Shen J.-P., and He J.-Z. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil?. Environmental Microbiology 10 (2008) 1978-1987
26. Coolen M.J.L., Abbas B., Van Bleijswijk J., Hopmans E.C., Kuypers M.M.M., Wakeham S.G., and Sinninghe Damste J.S. 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. Environmental Microbiology 9 (2007) 1001-1016
27. Crump B.C., Hopkinson C.S., Sogin M.L., and Hobbie J.E. Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time. Applied and Environmental Microbiology 70 (2004) 1494-1505
28. DeLong E.F. Archaea in coastal marine environments. Proceedings of the National Academy of Science of the United States of America 89 (1992) 5685-5689
29. Dollhopf S.L., Hyun J.-H., Smith A.C., Adams H.J., O'Brien S., and Kostka J.E. Quantification of ammonia-oxidizing bacteria and factors controlling nitrification in salt marsh sediments. Applied and Environmental Microbiology 71 (2005) 240-246
30. Francis C.A., O'Mullan G.D., and Ward B.B. Diversity of ammonia monooxygenase (amoA) genes across environmental gradients in Chesapeake Bay sediments. Geobiology 1 (2003) 129-140
31. Francis C.A., Roberts K.J., Beman J.M., Santoro A.E., and 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 102 (2005) 14683-14688
32. Freitag T.E., Chang L., and Prosser J.I. Changes in the community structure and activity of betaproteobacterial ammonia-oxidizing sediment bacteria along a freshwater-marine gradient. Environmental Microbiology 8 (2006) 684-696
33. Fuhrman J.A., McCallum K., and Davies A.A. Novel major archaebacterial group from marine plankton. Nature 356 (1992) 148-149
34. Gieseke A., Purkhold U., Wagner M., Amann R., and Schramm A. Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Applied and Environmental Microbiology 67 (2001) 1351-1362
35. Hallam S.J., Konstantinidis K.T., Putnam N., Schleper C., Watanabe Y.I., Sugahara J., Preston C., De La Torre J., Richardson P.M., and DeLong E.F. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 18296-18301
36. Hatzenpichler R., Lebedeva E.V., Spieck E., Stoecker K., Richter A., Daims H., and Wagner M. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Sciences of the United States of America 105 (2008) 2134-2139
37. Head I.M., Hiorns W.D., Embley T.M., McCarthy A.J., and Saunders J.R. The phylogeny of autotrophic ammonia-oxidizing bacteria as determined by analysis of 16S ribosomal-RNA gene-sequences. Journal of General Microbiology 139 (1993) 1147-1153
38. Henriksen K. Measurement of in situ rates of nitrification in sediment. Microbial Ecology 6 (1980) 329-337
39. Herndl G.J., Reinthaler T., Teira E., van Aken H., Veth C., Pernthaler A., and Pernthaler J. Contribution of archaea to total prokaryotic production in the deep Atlantic Ocean. Applied and Environmental Microbiology 71 (2005) 2303-2309
40. Hewson I., and Fuhrman J.A. Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Applied and Environmental Microbiology 70 (2004) 3425-3433
41. Holmes A.J., Costello A., Lidstrom M.E., and Murrell J.C. Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiology Letters 132 (1995) 203-208
42. Hommes N.G., Sayavedra-Soto L.A., and Arp D.J. Chemoorganotrophic growth of Nitrosomonas europaea on fructose. Journal of Bacteriology 185 (2003) 6809-6814
43. Hornek R., Pommerening-Roser A., Koops H.P., Farnleitner A.H., Kreuzinger N., Kirschner A., and Mach R.L. Primers containing universal bases reduce multiple amoA gene specific DGGE band patterns when analysing the diversity of beta-ammonia oxidizers in the environment. Journal of Microbiological Methods 66 (2006) 147-155
44. Howarth R.W. Nutrient limitation of net primary production in marine ecosystems. Annual Reviews in Ecology 19 (1988) 89-110
45. Ingalls A.E., Shah S.R., Hansman R.L., Aluwihare L.I., Santos G.M., Druffel E.R.M., and Pearson A. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 6442-6447
46. Jenkins M.C., and Kemp W.M. The coupling of nitrification and denitrification in two estuarine sediments. Limnology and Oceanography 29 (1984) 609-619
47. Jia Z., and Conrad R. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environmental Microbiology 11 (2009) 1658-1671
48. Karner M.B., DeLong E.F., and Karl D.M. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409 (2001) 507-510
49. Könneke M., Bernhard A.E., de la Torre J.R., Walker C.B., Waterbury J.B., and Stahl D.A. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437 (2005) 543-546
50. Koops H.P., and Pommerening-Roser A. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiology Ecology 37 (2001) 1-9
51. Kowalchuk G.A., and Stephen J.R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annual Reviews in Microbiology 55 (2001) 485-529
52. Lam P., Jensen M.M., Lavik G., McGinnis D.F., Muller B., Schubert C.J., Amann R., Thamdrup B., and 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 104 (2007) 7104-7109
53. Leininger S., Urich T., Schloter M., Schwark L., Qi J., Nicol G.W., Prosser J.I., Schuster S.C., and Schleper C. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442 (2006) 806-809
54. MacGregor B.J., Moser D.P., Alm E.W., Nealson K.H., and Stahl D.A. Crenarchaeota in Lake Michigan. Applied and Environmental Microbiology 63 (1997) 1178-1181
55. Martens-Habbena W., Berube P.M., Urakawa H., de la Torre J.R., and Stahl D.A. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461 (2009) 976-981
56. Mendelssohn I.A., McKee K.L., and Patrick Jr. W.H. Oxygen deficiency in Spartina alterniflora roots: metabolic adaptation to anoxia. Science 214 (1981) 439-441
57. Mincer T.J., Church M.J., Taylor L.T., Preston C., Karl D.M., and DeLong E.F. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey bay and the North Pacific subtropical Gyre. Environmental Microbiology 9 (2007) 1162-1175
58. Moin N.S., Nelson K.A., Bush A., and Bernhard A.E. Distribution and diversity of archaeal and bacterial ammonia oxidizers in salt marsh sediments. Applied and Environmental Microbiology 75 (2009) 7461-7468
59. Mosier A.C., and Francis C.A. Relative abundance and diversity of ammonia-oxidizing archaea and bacteria in the San Francisco Bay estuary. Environmental Microbiology 10 (2008) 3002-3016
60. Nicol G.W., Leininger S., Schleper C., and Prosser J.I. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxiizing archaea and bacteria. Environmental Microbiology 10 (2008) 2966-2978
61. Nold S.C., Zhou J., Devol A.H., and Tiedje J.M. Pacific Northwest marine sediments contain ammonia-oxidizing bacteria in the β subdivision of the Proteobacteria. Applied and Environmental Microbiology 66 (2000) 4532-4535
62. O'Mullan G.D., and Ward B.B. Relationship of temporal and spatial variabilities of ammonia-oxidizing bacteria to nitrification rates in Monterrey Bay, California. Applied and Environmental Microbiology 71 (2005) 697-705
63. Ouverney C.C., and Fuhrman J.A. Marine planktonic archaea take up amino acids. Applied and Environmental Microbiology 66 (2000) 4829-4833
64. Oved T., Shaviv A., Goldrath T., Mandelbaum R.T., and Minz D. Influence of effluent irrigation on community composition and function of ammonia-oxidizing bacteria in soil. Applied and Environmental Microbiology 67 (2001) 3426-3433
65. Pace N.R., Stahl D.A., Lane D.J., and Olsen G.J. The analysis of natural microbial populations by ribosomal RNA sequences. Advances in Microbial Ecology 9 (1986) 1-55
66. Park S.J., Park B.J., and Rhee S.K. Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments. Extremophiles (2008) 1-11
67. 14C analysis. Geochimica Cosmochimica Acta 65 (2001) 3123-3137
68. Prosser J.I. Autotrophic nitrification in bacteria. Advances in Microbial Physiology 30 (1989) 125-181
69. Prosser J.I., and Nicol G.W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environmental Microbiology 10 (2008) 2931-2941
70. Purkhold U., Pommerening-Roser A., Juretschko S., Schmid M.C., Koops H.P., and Wagner M. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Applied and Environmental Microbiology 66 (2000) 5368-5382
71. Risgaard-Petersen N., Nicolaisen M.H., Revsbech N.P., and Lomstein B.A. Competition between ammonia-oxidizing bacteria and benthic microalgae. Applied and Environmental Microbiology 70 (2004) 5528-5537
72. Rotthauwe J.H., Witzel K.P., and 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 63 (1997) 4704-4712
73. + adsorption capacity, nitrification, and denitrification in Danish estuarine sediments. Estuaries 22 (1999) 21-30
74. Sahan E., and Muyzer G. Diversity and spatio-temporal distribution of ammonia-oxidizing archaea and bacteria in sediments of the Westerschelde estuary. FEMS Microbiology Ecology 64 (2008) 175-186
75. Santoro A.E., Francis C.A., De Sieyes N.R., and Boehm A.B. Shifts in the relative abundance of ammonia-oxidizing bacteria and archaea across physicochemical gradients in a subterranean estuary. Environmental Microbiology 10 (2008) 1068-1079
76. Schauss K., Focks A., Leininger S., Kotzerke A., Heuer H., Thiele-Bruhn S., Sharma S., Wilke B.-M., Matthies M., Smalla K., Munch J.C., Amelung W., Kaupenjohann M., Schloter M., and Schleper C. Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environmental Microbiology 11 (2009) 446-456
77. Schramm A., De Beer D., Gieseke A., and Amann R. Microenvironments and distribution of nitrifying bacteria in a membrane-bound biofilm. Environmental Microbiology 2 (2000) 680-686
78. Sebilo M., Billen G., Mayer B., Billiou D., Grably M., Garnier J., and Mariotti A. Assessing nitrification and denitrification in the Seine River and estuary using chemical and isotopic techniques. Ecosystems 9 (2006) 564-577
79. Seitzinger S.P. Denitrification infresh-water and coastal marine ecosystems - ecological and geochemical significance. Limnology and Oceanography 33 (1988) 702-724
80. Stehr G., Bottcher B., Dittberner P., Rath G., and Koops H.-P. The ammonia-oxidizing nitrifying population of the River Elbe estuary. FEMS Microbiology Ecology 17 (1995) 177-186
81. Suwa Y., Sumino T., and Noto K. Phylogenetic relationships of activated sludge isolates of ammonia oxidizers with different sensitivities to ammonium sulfate. Journal of General and Applied Microbiology 43 (1997) 373-379
82. Suzuki M.T., Rappe M.S., and Giovannoni S.J. Kinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small subunit rRNA gene PCR amplicon length heterogeneity. Applied and Environmental Microbiology 64 (1998) 4522-4529
83. Teira E., van Aken H., Veth C., and Herndl G.J. Archaeal uptake of enantiomeric amino acids in the meso- and bathypelagic waters of the North Atlantic. Limnology and Oceanography 51 (2006) 60-69
84. Thompson S.P., Paerl H.W., and Go M.C. Seasonal patterns of nitrification and denitrification in a natural and a restored salt marsh. Estuaries 18 (1995) 399-408
85. Tobias C.R., Anderson I.C., Canuel E.A., and Macko S.A. Nitrogen cycling through a fringing marsh-aquifer ecotone. Marine Ecology Progress Series 210 (2001) 25-39
86. Treusch A.H., Leininger S., Kietzin A., Schuster S.C., Klenk H.P., and Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic Crenarchaeota in nitrogen cycling. Environmental Microbiology 7 (2005) 1985-1995
87. Urakawa H., Kurata S., Fujiwara T., Kuroiwa D., Maki H., Kawabata S., Hiwatari T., Ando H., Kawai T., Watanabe M., and Kohata K. Characterization and quantification of ammonia-oxidizing bacteria in eutrophic coastal marine sediments using polyphasic molecular approaches and immunofluorescence staining. Environmental Microbiology 8 (2006) 787-803
88. Urakawa H., Tajima Y., Numata Y., and Tsuneda S. Low temperature decreases the phylogenetic diversity of ammonia-oxidizing archaea and bacteria in aquarium biofiltration systems. Applied and Environmental Microbiology 74 (2008) 894-900
89. Utaker J.B., and Nes I.F. A qualitative evaluation of the published oligonucleotides specific for the 16S rRNA gene sequences of the ammonia-oxidizing bacteria. Systematic and Applied Microbiology 21 (1998) 72-88
90. Venter J.C., Remington K., Heidelberg J.F., Halpern A.L., Rusch D., Eisen J.A., Wu D., Paulsen I., Nelson K.E., Nelson W., Fouts D.E., Levy S., Knap A.H., Lomas M.W., Nealson K., White O., Peterson J., Hoffman J., Parsons R., Baden-Tillson H., Pfannkoch C., Rogers Y.-H., and Smith H.O. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304 (2004) 66-74
91. Ward B.B., Eveillard D., Kirshtein J.D., Nelson J.D., Voytek M.A., and Jackson G.A. Ammonia-oxidizing bacterial community composition in estuarine and oceanic environments assessed using a functional gene microarray. Environmental Microbiology 9 (2007) 2522-2538
92. Watson S.W. Characteristics of a marine nitrifying bacterium, Nitrosocystis oceanus sp. N. Limnology and Oceanography 10 Suppl. (1965) 274-289
93. Weidler G.W., Dornmayr-Pfaffenhuemer M., Gerbl F.W., Heinen W., and Stan-Lotter H. Communities of archaea and bacteria in a subsurface radioactive thermal spring in the Austrian central alps, and evidence of ammonia-oxidizing Crenarchaeota. Applied and Environmental Microbiology 73 (2007) 259-270
94. Woese C.R., Weisburg W.G., and Paster B.J. The purple bacteria: the beta subdivision. Systematic and Applied Microbiology 5 (1984) 327-336
95. Woese C.R., Weisburg W.G., and Hahn C.M. The purple bacteria: the gamma subdivision. Systematic and Applied Microbiology 6 (1985) 25-33
96. Wuchter C., Schouten S., Boschker H.T.S., and Sinninghe Damsté J.S. Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiology Letters 219 (2003) 203-207
97. Wuchter C., Abbas B., Coolen M.J.L., Herfort L., Van Bleijswijk J., Timmers P., Strous M., Teira E., Herndl G.J., Middelburg J.J., Schouten S., and Sinninghe Damsté J.S. Archaeal nitrification in the ocean. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 12317-12322