Previous Article | Next Article 
Applied and Environmental Microbiology, December 2000, p. 5368-5382, Vol. 66, No. 12
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Phylogeny of All Recognized Species of Ammonia Oxidizers Based on
Comparative 16S rRNA and amoA Sequence Analysis:
Implications for Molecular Diversity Surveys
Ulrike
Purkhold,1
Andreas
Pommerening-Röser,2
Stefan
Juretschko,1
Markus C.
Schmid,1
Hans-Peter
Koops,2 and
Michael
Wagner1,*
Lehrstuhl für Mikrobiologie, Technische
Universität München, D-85350
Freising,1 Institut für allgemeine
Botanik, Abteilung Mikrobiologie, Universität Hamburg, D-22609
Hamburg,2 Germany
Received 17 July 2000/Accepted 4 October 2000
The current perception of evolutionary relationships and the
natural diversity of ammonia-oxidizing bacteria (AOB) is mainly based
on comparative sequence analyses of their genes encoding the 16S rRNA
and the active site polypeptide of the ammonia monooxygenase (AmoA).
However, only partial 16S rRNA sequences are available for many AOB
species and most AOB have not yet been analyzed on the amoA
level. In this study, the 16S rDNA sequence data of 10 Nitrosomonas species and Nitrosococcus mobilis
were completed. Furthermore, previously unavailable 16S rRNA sequences
were determined for three Nitrosomonas sp. isolates and for
the gamma-subclass proteobacterium Nitrosococcus
halophilus. These data were used to revaluate the specificities
of published oligonucleotide primers and probes for AOB. In addition,
partial amoA sequences of 17 AOB, including the
above-mentioned 15 AOB, were obtained. Comparative phylogenetic
analyses suggested similar but not identical evolutionary relationships
of AOB by using 16S rRNA and AmoA as marker molecules, respectively.
The presented 16S rRNA and amoA and AmoA sequence data from
all recognized AOB species significantly extend the currently used
molecular classification schemes for AOB and now provide a more robust
phylogenetic framework for molecular diversity inventories of AOB. For
16S rRNA-independent evaluation of AOB species-level diversity in
environmental samples, amoA and AmoA sequence similarity
threshold values were determined which can be used to tentatively
identify novel species based on cloned amoA sequences.
Subsequently, 122 amoA sequences were obtained from 11 nitrifying wastewater treatment plants. Phylogenetic analyses of the
molecular isolates showed that in all but two plants only nitrosomonads
could be detected. Although several of the obtained amoA
sequences were only relatively distantly related to known AOB, none of
these sequences unequivocally suggested the existence of previously
unrecognized species in the wastewater treatment environments examined.
*
Corresponding author. Mailing address: Lehrstuhl
für Mikrobiologie, Technische Universität München, Am
Hochanger 4, D-85350 Freising, Germany. Phone: 49 8161 71 5444. Fax: 49 8161 71 5475. E-mail:
wagner{at}mikro.biologie.tu-muenchen.de.
Applied and Environmental Microbiology, December 2000, p. 5368-5382, Vol. 66, No. 12
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Junier, P., Kim, O.-S., Hadas, O., Imhoff, J. F., Witzel, K.-P.
(2008). Evaluation of PCR Primer Selectivity and Phylogenetic Specificity by Using Amplification of 16S rRNA Genes from Betaproteobacterial Ammonia-Oxidizing Bacteria in Environmental Samples. Appl. Environ. Microbiol.
74: 5231-5236
[Abstract]
[Full Text]
-
McDonald, I. R., Bodrossy, L., Chen, Y., Murrell, J. C.
(2008). Molecular Ecology Techniques for the Study of Aerobic Methanotrophs. Appl. Environ. Microbiol.
74: 1305-1315
[Full Text]
-
Hatzenpichler, R., Lebedeva, E. V., Spieck, E., Stoecker, K., Richter, A., Daims, H., Wagner, M.
(2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. USA
105: 2134-2139
[Abstract]
[Full Text]
-
Lebedeva, E. V., Alawi, M., Maixner, F., Jozsa, P.-G., Daims, H., Spieck, E.
(2008). Physiological and phylogenetic characterization of a novel lithoautotrophic nitrite-oxidizing bacterium, 'Candidatus Nitrospira bockiana'. Int. J. Syst. Evol. Microbiol.
58: 242-250
[Abstract]
[Full Text]
-
Cherif-Zahar, B., Durand, A., Schmidt, I., Hamdaoui, N., Matic, I., Merrick, M., Matassi, G.
(2007). Evolution and Functional Characterization of the RH50 Gene from the Ammonia-Oxidizing Bacterium Nitrosomonas europaea. J. Bacteriol.
189: 9090-9100
[Abstract]
[Full Text]
-
He, S., Gall, D. L., McMahon, K. D.
(2007). "Candidatus Accumulibacter" Population Structure in Enhanced Biological Phosphorus Removal Sludges as Revealed by Polyphosphate Kinase Genes. Appl. Environ. Microbiol.
73: 5865-5874
[Abstract]
[Full Text]
-
Taylor, M. W., Radax, R., Steger, D., Wagner, M.
(2007). Sponge-Associated Microorganisms: Evolution, Ecology, and Biotechnological Potential. Microbiol. Mol. Biol. Rev.
71: 295-347
[Abstract]
[Full Text]
-
Pernice, M., Wetzel, S., Gros, O., Boucher-Rodoni, R., Dubilier, N.
(2007). Enigmatic dual symbiosis in the excretory organ of Nautilus macromphalus (Cephalopoda: Nautiloidea). Proc R Soc B
274: 1143-1152
[Abstract]
[Full Text]
-
Avrahami, S., Bohannan, B. J. M.
(2007). Response of Nitrosospira sp. Strain AF-Like Ammonia Oxidizers to Changes in Temperature, Soil Moisture Content, and Fertilizer Concentration. Appl. Environ. Microbiol.
73: 1166-1173
[Abstract]
[Full Text]
-
Chu, H., Fujii, T., Morimoto, S., Lin, X., Yagi, K., Hu, J., Zhang, J.
(2007). Community Structure of Ammonia-Oxidizing Bacteria under Long-Term Application of Mineral Fertilizer and Organic Manure in a Sandy Loam Soil. Appl. Environ. Microbiol.
73: 485-491
[Abstract]
[Full Text]
-
Urakawa, H., Maki, H., Kawabata, S., Fujiwara, T., Ando, H., Kawai, T., Hiwatari, T., Kohata, K., Watanabe, M.
(2006). Abundance and population structure of ammonia-oxidizing bacteria that inhabit canal sediments receiving effluents from municipal wastewater treatment plants.. Appl. Environ. Microbiol.
72: 6845-6850
[Abstract]
[Full Text]
-
Hunter, E. M., Mills, H. J., Kostka, J. E.
(2006). Microbial Community Diversity Associated with Carbon and Nitrogen Cycling in Permeable Shelf Sediments. Appl. Environ. Microbiol.
72: 5689-5701
[Abstract]
[Full Text]
-
Park, H.-D., Wells, G. F., Bae, H., Criddle, C. S., Francis, C. A.
(2006). Occurrence of Ammonia-Oxidizing Archaea in Wastewater Treatment Plant Bioreactors. Appl. Environ. Microbiol.
72: 5643-5647
[Abstract]
[Full Text]
-
Gieseke, A., Tarre, S., Green, M., de Beer, D.
(2006). Nitrification in a Biofilm at Low pH Values: Role of In Situ Microenvironments and Acid Tolerance.. Appl. Environ. Microbiol.
72: 4283-4292
[Abstract]
[Full Text]
-
Mota, C., Head, M. A., Ridenoure, J. A., Cheng, J. J., de los Reyes, F. L. III
(2005). Effects of Aeration Cycles on Nitrifying Bacterial Populations and Nitrogen Removal in Intermittently Aerated Reactors. Appl. Environ. Microbiol.
71: 8565-8572
[Abstract]
[Full Text]
-
Simbahan, J., Kurth, E., Schelert, J., Dillman, A., Moriyama, E., Jovanovich, S., Blum, P.
(2005). Community Analysis of a Mercury Hot Spring Supports Occurrence of Domain-Specific Forms of Mercuric Reductase. Appl. Environ. Microbiol.
71: 8836-8845
[Abstract]
[Full Text]
-
Coskuner, G., Ballinger, S. J., Davenport, R. J., Pickering, R. L., Solera, R., Head, I. M., Curtis, T. P.
(2005). Agreement between Theory and Measurement in Quantification of Ammonia-Oxidizing Bacteria. Appl. Environ. Microbiol.
71: 6325-6334
[Abstract]
[Full Text]
-
Bergmann, D. J., Hooper, A. B., Klotz, M. G.
(2005). Structure and Sequence Conservation of hao Cluster Genes of Autotrophic Ammonia-Oxidizing Bacteria: Evidence for Their Evolutionary History. Appl. Environ. Microbiol.
71: 5371-5382
[Abstract]
[Full Text]
-
Yeager, C. M., Northup, D. E., Grow, C. C., Barns, S. M., Kuske, C. R.
(2005). Changes in Nitrogen-Fixing and Ammonia-Oxidizing Bacterial Communities in Soil of a Mixed Conifer Forest after Wildfire. Appl. Environ. Microbiol.
71: 2713-2722
[Abstract]
[Full Text]
-
Spring, S., Wagner, M., Schumann, P., Kampfer, P.
(2005). Malikia granosa gen. nov., sp. nov., a novel polyhydroxyalkanoate- and polyphosphate-accumulating bacterium isolated from activated sludge, and reclassification of Pseudomonas spinosa as Malikia spinosa comb. nov.. Int. J. Syst. Evol. Microbiol.
55: 621-629
[Abstract]
[Full Text]
-
Bollmann, A., Schmidt, I., Saunders, A. M., Nicolaisen, M. H.
(2005). Influence of Starvation on Potential Ammonia-Oxidizing Activity and amoA mRNA Levels of Nitrosospira briensis. Appl. Environ. Microbiol.
71: 1276-1282
[Abstract]
[Full Text]
-
Loy, A., Schulz, C., Lucker, S., Schopfer-Wendels, A., Stoecker, K., Baranyi, C., Lehner, A., Wagner, M.
(2005). 16S rRNA Gene-Based Oligonucleotide Microarray for Environmental Monitoring of the Betaproteobacterial Order "Rhodocyclales". Appl. Environ. Microbiol.
71: 1373-1386
[Abstract]
[Full Text]
-
Yu, C.-P., Ahuja, R., Sayler, G., Chu, K.-H.
(2005). Quantitative Molecular Assay for Fingerprinting Microbial Communities of Wastewater and Estrogen-Degrading Consortia. Appl. Environ. Microbiol.
71: 1433-1444
[Abstract]
[Full Text]
-
O'Mullan, G. D., Ward, B. B.
(2005). Relationship of Temporal and Spatial Variabilities of Ammonia-Oxidizing Bacteria to Nitrification Rates in Monterey Bay, California. Appl. Environ. Microbiol.
71: 697-705
[Abstract]
[Full Text]
-
Layton, A. C., Dionisi, H., Kuo, H.-W., Robinson, K. G., Garrett, V. M., Meyers, A., Sayler, G. S.
(2005). Emergence of Competitive Dominant Ammonia-Oxidizing Bacterial Populations in a Full-Scale Industrial Wastewater Treatment Plant. Appl. Environ. Microbiol.
71: 1105-1108
[Abstract]
[Full Text]
-
Selesi, D., Schmid, M., Hartmann, A.
(2005). Diversity of Green-Like and Red-Like Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Large-Subunit Genes (cbbL) in Differently Managed Agricultural Soils. Appl. Environ. Microbiol.
71: 175-184
[Abstract]
[Full Text]
-
Jordan, F. L., Cantera, J. J. L., Fenn, M. E., Stein, L. Y.
(2005). Autotrophic Ammonia-Oxidizing Bacteria Contribute Minimally to Nitrification in a Nitrogen-Impacted Forested Ecosystem. Appl. Environ. Microbiol.
71: 197-206
[Abstract]
[Full Text]
-
Loy, A., Kusel, K., Lehner, A., Drake, H. L., Wagner, M.
(2004). Microarray and Functional Gene Analyses of Sulfate-Reducing Prokaryotes in Low-Sulfate, Acidic Fens Reveal Cooccurrence of Recognized Genera and Novel Lineages. Appl. Environ. Microbiol.
70: 6998-7009
[Abstract]
[Full Text]
-
Nielsen, J. L., Schramm, A., Bernhard, A. E., van den Engh, G. J., Stahl, D. A.
(2004). Flow Cytometry-Assisted Cloning of Specific Sequence Motifs from Complex 16S rRNA Gene Libraries. Appl. Environ. Microbiol.
70: 7550-7554
[Abstract]
[Full Text]
-
Cebron, A., Coci, M., Garnier, J., Laanbroek, H. J.
(2004). Denaturing Gradient Gel Electrophoretic Analysis of Ammonia-Oxidizing Bacterial Community Structure in the Lower Seine River: Impact of Paris Wastewater Effluents. Appl. Environ. Microbiol.
70: 6726-6737
[Abstract]
[Full Text]
-
Risgaard-Petersen, N., Nicolaisen, M. H., Revsbech, N. P., Lomstein, B. A.
(2004). Competition between Ammonia-Oxidizing Bacteria and Benthic Microalgae. Appl. Environ. Microbiol.
70: 5528-5537
[Abstract]
[Full Text]
-
Freitag, T. E., Prosser, J. I.
(2004). Differences between Betaproteobacterial Ammonia-Oxidizing Communities in Marine Sediments and Those in Overlying Water. Appl. Environ. Microbiol.
70: 3789-3793
[Abstract]
[Full Text]
-
Cole, A. C., Semmens, M. J., LaPara, T. M.
(2004). Stratification of Activity and Bacterial Community Structure in Biofilms Grown on Membranes Transferring Oxygen. Appl. Environ. Microbiol.
70: 1982-1989
[Abstract]
[Full Text]
-
Nanba, K., King, G. M., Dunfield, K.
(2004). Analysis of Facultative Lithotroph Distribution and Diversity on Volcanic Deposits by Use of the Large Subunit of Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase. Appl. Environ. Microbiol.
70: 2245-2253
[Abstract]
[Full Text]
-
Koper, T. E., El-Sheikh, A. F., Norton, J. M., Klotz, M. G.
(2004). Urease-Encoding Genes in Ammonia-Oxidizing Bacteria. Appl. Environ. Microbiol.
70: 2342-2348
[Abstract]
[Full Text]
-
Cebron, A., Berthe, T., Garnier, J.
(2003). Nitrification and Nitrifying Bacteria in the Lower Seine River and Estuary (France). Appl. Environ. Microbiol.
69: 7091-7100
[Abstract]
[Full Text]
-
Adamczyk, J., Hesselsoe, M., Iversen, N., Horn, M., Lehner, A., Nielsen, P. H., Schloter, M., Roslev, P., Wagner, M.
(2003). The Isotope Array, a New Tool That Employs Substrate-Mediated Labeling of rRNA for Determination of Microbial Community Structure and Function. Appl. Environ. Microbiol.
69: 6875-6887
[Abstract]
[Full Text]
-
Avrahami, S., Conrad, R.
(2003). Patterns of Community Change among Ammonia Oxidizers in Meadow Soils upon Long-Term Incubation at Different Temperatures. Appl. Environ. Microbiol.
69: 6152-6164
[Abstract]
[Full Text]
-
Ibekwe, A. M., Grieve, C. M., Lyon, S. R.
(2003). Characterization of Microbial Communities and Composition in Constructed Dairy Wetland Wastewater Effluent. Appl. Environ. Microbiol.
69: 5060-5069
[Abstract]
[Full Text]
-
Bent, S. J., Gucker, C. L., Oda, Y., Forney, L. J.
(2003). Spatial Distribution of Rhodopseudomonas palustris Ecotypes on a Local Scale. Appl. Environ. Microbiol.
69: 5192-5197
[Abstract]
[Full Text]
-
Purkhold, U., Wagner, M., Timmermann, G., Pommerening-Roser, A., Koops, H.-P.
(2003). 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int. J. Syst. Evol. Microbiol.
53: 1485-1494
[Abstract]
[Full Text]
-
Mintie, A. T., Heichen, R. S., Cromack, K. Jr., Myrold, D. D., Bottomley, P. J.
(2003). Ammonia-Oxidizing Bacteria along Meadow-to-Forest Transects in the Oregon Cascade Mountains. Appl. Environ. Microbiol.
69: 3129-3136
[Abstract]
[Full Text]
-
Egli, K., Langer, C., Siegrist, H.-R., Zehnder, A. J. B., Wagner, M., van der Meer, J. R.
(2003). Community Analysis of Ammonia and Nitrite Oxidizers during Start-Up of Nitritation Reactors. Appl. Environ. Microbiol.
69: 3213-3222
[Abstract]
[Full Text]
-
Boon, N., Top, E. M., Verstraete, W., Siciliano, S. D.
(2003). Bioaugmentation as a Tool To Protect the Structure and Function of an Activated-Sludge Microbial Community against a 3-Chloroaniline Shock Load. Appl. Environ. Microbiol.
69: 1511-1520
[Abstract]
[Full Text]
-
Avrahami, S., Conrad, R., Braker, G.
(2002). Effect of Soil Ammonium Concentration on N2O Release and on the Community Structure of Ammonia Oxidizers and Denitrifiers. Appl. Environ. Microbiol.
68: 5685-5692
[Abstract]
[Full Text]
-
Bollmann, A., Bar-Gilissen, M.-J., Laanbroek, H. J.
(2002). Growth at Low Ammonium Concentrations and Starvation Response as Potential Factors Involved in Niche Differentiation among Ammonia-Oxidizing Bacteria. Appl. Environ. Microbiol.
68: 4751-4757
[Abstract]
[Full Text]
-
Loy, A., Lehner, A., Lee, N., Adamczyk, J., Meier, H., Ernst, J., Schleifer, K.-H., Wagner, M.
(2002). Oligonucleotide Microarray for 16S rRNA Gene-Based Detection of All Recognized Lineages of Sulfate-Reducing Prokaryotes in the Environment. Appl. Environ. Microbiol.
68: 5064-5081
[Abstract]
[Full Text]
-
Heyer, J., Galchenko, V. F., Dunfield, P. F.
(2002). Molecular phylogeny of type II methane-oxidizing bacteria isolated from various environments. Microbiology
148: 2831-2846
[Abstract]
[Full Text]
-
Curtis, T. P., Sloan, W. T., Scannell, J. W.
(2002). From the Cover: Estimating prokaryotic diversity and its limits. Proc. Natl. Acad. Sci. USA
99: 10494-10499
[Abstract]
[Full Text]
-
Briones, A. M., Okabe, S., Umemiya, Y., Ramsing, N.-B., Reichardt, W., Okuyama, H.
(2002). Influence of Different Cultivars on Populations of Ammonia-Oxidizing Bacteria in the Root Environment of Rice. Appl. Environ. Microbiol.
68: 3067-3075
[Abstract]
[Full Text]
-
Sakano, Y., Pickering, K. D., Strom, P. F., Kerkhof, L. J.
(2002). Spatial Distribution of Total, Ammonia-Oxidizing, and Denitrifying Bacteria in Biological Wastewater Treatment Reactors for Bioregenerative Life Support. Appl. Environ. Microbiol.
68: 2285-2293
[Abstract]
[Full Text]
-
Zehr, J. P., Ward, B. B.
(2002). Nitrogen Cycling in the Ocean: New Perspectives on Processes and Paradigms. Appl. Environ. Microbiol.
68: 1015-1024
[Full Text]
-
Hollibaugh, J. T., Bano, N., Ducklow, H. W.
(2002). Widespread Distribution in Polar Oceans of a 16S rRNA Gene Sequence with Affinity to Nitrosospira-Like Ammonia-Oxidizing Bacteria. Appl. Environ. Microbiol.
68: 1478-1484
[Abstract]
[Full Text]
-
Regan, J. M., Harrington, G. W., Noguera, D. R.
(2002). Ammonia- and Nitrite-Oxidizing Bacterial Communities in a Pilot-Scale Chloraminated Drinking Water Distribution System. Appl. Environ. Microbiol.
68: 73-81
[Abstract]
[Full Text]
-
Dionisi, H. M., Layton, A. C., Harms, G., Gregory, I. R., Robinson, K. G., Sayler, G. S.
(2002). Quantification of Nitrosomonas oligotropha-Like Ammonia-Oxidizing Bacteria and Nitrospira spp. from Full-Scale Wastewater Treatment Plants by Competitive PCR. Appl. Environ. Microbiol.
68: 245-253
[Abstract]
[Full Text]
-
Burrell, P. C., Phalen, C. M., Hovanec, T. A.
(2001). Identification of Bacteria Responsible for Ammonia Oxidation in Freshwater Aquaria. Appl. Environ. Microbiol.
67: 5791-5800
[Abstract]
[Full Text]
-
Daims, H., Ramsing, N. B., Schleifer, K.-H., Wagner, M.
(2001). Cultivation-Independent, Semiautomatic Determination of Absolute Bacterial Cell Numbers in Environmental Samples by Fluorescence In Situ Hybridization. Appl. Environ. Microbiol.
67: 5810-5818
[Abstract]
[Full Text]
-
Daims, H., Nielsen, J. L., Nielsen, P. H., Schleifer, K.-H., Wagner, M.
(2001). In Situ Characterization of Nitrospira-Like Nitrite-Oxidizing Bacteria Active in Wastewater Treatment Plants. Appl. Environ. Microbiol.
67: 5273-5284
[Abstract]
[Full Text]
-
Klein, M., Friedrich, M., Roger, A. J., Hugenholtz, P., Fishbain, S., Abicht, H., Blackall, L. L., Stahl, D. A., Wagner, M.
(2001). Multiple Lateral Transfers of Dissimilatory Sulfite Reductase Genes between Major Lineages of Sulfate-Reducing Prokaryotes. J. Bacteriol.
183: 6028-6035
[Abstract]
[Full Text]
-
Bourne, D. G., McDonald, I. R., Murrell, J. C.
(2001). Comparison of pmoA PCR Primer Sets as Tools for Investigating Methanotroph Diversity in Three Danish Soils. Appl. Environ. Microbiol.
67: 3802-3809
[Abstract]
[Full Text]
-
Oved, T., Shaviv, A., Goldrath, T., Mandelbaum, R. T., Minz, D.
(2001). Influence of Effluent Irrigation on Community Composition and Function of Ammonia-Oxidizing Bacteria in Soil. Appl. Environ. Microbiol.
67: 3426-3433
[Abstract]
[Full Text]
-
Casciotti, K. L., Ward, B. B.
(2001). Dissimilatory Nitrite Reductase Genes from Autotrophic Ammonia-Oxidizing Bacteria. Appl. Environ. Microbiol.
67: 2213-2221
[Abstract]
[Full Text]
-
Gieseke, A., Purkhold, U., Wagner, M., Amann, R., Schramm, A.
(2001). Community Structure and Activity Dynamics of Nitrifying Bacteria in a Phosphate-Removing Biofilm. Appl. Environ. Microbiol.
67: 1351-1362
[Abstract]
[Full Text]