Previous Article | Next Article 
Journal of Bacteriology, May 2003, p. 2759-2773, Vol. 185, No. 9
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.9.2759-2773.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
Complete Genome Sequence of the Ammonia-Oxidizing Bacterium and Obligate Chemolithoautotroph Nitrosomonas europaea
Patrick Chain,1,2 Jane Lamerdin,1,2 Frank Larimer,1,3 Warren Regala,1,2 Victoria Lao,1,2 Miriam Land,1,3 Loren Hauser,1,3 Alan Hooper,4 Martin Klotz,5 Jeanette Norton,6 Luis Sayavedra-Soto,7 Dave Arciero,4 Norman Hommes,7 Mark Whittaker,4 and Daniel Arp7*
Joint Genome Institute, Walnut Creek, California 94598,1
Lawrence Livermore National Laboratory, Livermore, California 94550,2
Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831,3
University of Minnesota, Minneapolis, Minnesota 55455,4
University of Louisville, Louisville, Kentucky 40208,5
Utah State University, Logan, Utah 84322,6
Oregon State University, Corvallis, Oregon 973317
Received 21 November 2002/
Accepted 20 February 2003
Nitrosomonas europaea (ATCC 19718) is a gram-negative obligate chemolithoautotroph that can derive all its energy and reductant for growth from the oxidation of ammonia to nitrite. Nitrosomonas europaea participates in the biogeochemical N cycle in the process of nitrification. Its genome consists of a single circular chromosome of 2,812,094 bp. The GC skew analysis indicates that the genome is divided into two unequal replichores. Genes are distributed evenly around the genome, with
47% transcribed from one strand and
53% transcribed from the complementary strand. A total of 2,460 protein-encoding genes emerged from the modeling effort, averaging 1,011 bp in length, with intergenic regions averaging 117 bp. Genes necessary for the catabolism of ammonia, energy and reductant generation, biosynthesis, and CO2 and NH3 assimilation were identified. In contrast, genes for catabolism of organic compounds are limited. Genes encoding transporters for inorganic ions were plentiful, whereas genes encoding transporters for organic molecules were scant. Complex repetitive elements constitute ca. 5% of the genome. Among these are 85 predicted insertion sequence elements in eight different families. The strategy of N. europaea to accumulate Fe from the environment involves several classes of Fe receptors with more than 20 genes devoted to these receptors. However, genes for the synthesis of only one siderophore, citrate, were identified in the genome. This genome has provided new insights into the growth and metabolism of ammonia-oxidizing bacteria.
* Corresponding author. Mailing address: Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331-2902. Phone: (541) 737-1294. Fax: (541) 737-5310. E-mail: arpd{at}bcc.orst.edu.
For a commentary on this article, see page 2690 in this issue.
Journal of Bacteriology, May 2003, p. 2759-2773, Vol. 185, No. 9
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.9.2759-2773.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Nawata, C. M., Wood, C. M.
(2008). The effects of CO2 and external buffering on ammonia excretion and Rhesus glycoprotein mRNA expression in rainbow trout. J. Exp. Biol.
211: 3226-3236
[Abstract]
[Full Text]
-
Norton, J. M., Klotz, M. G., Stein, L. Y., Arp, D. J., Bottomley, P. J., Chain, P. S. G., Hauser, L. J., Land, M. L., Larimer, F. W., Shin, M. W., Starkenburg, S. R.
(2008). Complete Genome Sequence of Nitrosospira multiformis, an Ammonia-Oxidizing Bacterium from the Soil Environment. Appl. Environ. Microbiol.
74: 3559-3572
[Abstract]
[Full Text]
-
Starkenburg, S. R., Larimer, F. W., Stein, L. Y., Klotz, M. G., Chain, P. S. G., Sayavedra-Soto, L. A., Poret-Peterson, A. T., Gentry, M. E., Arp, D. J., Ward, B., Bottomley, P. J.
(2008). Complete Genome Sequence of Nitrobacter hamburgensis X14 and Comparative Genomic Analysis of Species within the Genus Nitrobacter. Appl. Environ. Microbiol.
74: 2852-2863
[Abstract]
[Full Text]
-
Badger, M. R., Bek, E. J.
(2008). Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot
59: 1525-1541
[Abstract]
[Full Text]
-
Chandran, K., Love, N. G.
(2008). Physiological State, Growth Mode, and Oxidative Stress Play a Role in Cd(II)-Mediated Inhibition of Nitrosomonas europaea 19718. Appl. Environ. Microbiol.
74: 2447-2453
[Abstract]
[Full Text]
-
Sievert, S. M., Scott, K. M., Klotz, M. G., Chain, P. S. G., Hauser, L. J., Hemp, J., Hugler, M., Land, M., Lapidus, A., Larimer, F. W., Lucas, S., Malfatti, S. A., Meyer, F., Paulsen, I. T., Ren, Q., Simon, J., the USF Genomics Class,
(2008). Genome of the Epsilonproteobacterial Chemolithoautotroph Sulfurimonas denitrificans. Appl. Environ. Microbiol.
74: 1145-1156
[Abstract]
[Full Text]
-
El Sheikh, A. F., Poret-Peterson, A. T., Klotz, M. G.
(2008). Characterization of Two New Genes, amoR and amoD, in the amo Operon of the Marine Ammonia Oxidizer Nitrosococcus oceani ATCC 19707. Appl. Environ. Microbiol.
74: 312-318
[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]
-
Lupo, D., Li, X.-D., Durand, A., Tomizaki, T., Cherif-Zahar, B., Matassi, G., Merrick, M., Winkler, F. K.
(2007). The 1.3-A resolution structure of Nitrosomonas europaea Rh50 and mechanistic implications for NH3 transport by Rhesus family proteins. Proc. Natl. Acad. Sci. USA
104: 19303-19308
[Abstract]
[Full Text]
-
Li, X., Jayachandran, S., Nguyen, H.-H. T., Chan, M. K.
(2007). Structure of the Nitrosomonas europaea Rh protein. Proc. Natl. Acad. Sci. USA
104: 19279-19284
[Abstract]
[Full Text]
-
Wei, X., Sayavedra-Soto, L. A., Arp, D. J.
(2007). Characterization of the ferrioxamine uptake system of Nitrosomonas europaea. Microbiology
153: 3963-3972
[Abstract]
[Full Text]
-
Berube, P. M., Samudrala, R., Stahl, D. A.
(2007). Transcription of All amoC Copies Is Associated with Recovery of Nitrosomonas europaea from Ammonia Starvation. J. Bacteriol.
189: 3935-3944
[Abstract]
[Full Text]
-
Gvakharia, B. O., Permina, E. A., Gelfand, M. S., Bottomley, P. J., Sayavedra-Soto, L. A., Arp, D. J.
(2007). Global Transcriptional Response of Nitrosomonas europaea to Chloroform and Chloromethane. Appl. Environ. Microbiol.
73: 3440-3445
[Abstract]
[Full Text]
-
Kane, S. R., Chakicherla, A. Y., Chain, P. S. G., Schmidt, R., Shin, M. W., Legler, T. C., Scow, K. M., Larimer, F. W., Lucas, S. M., Richardson, P. M., Hristova, K. R.
(2007). Whole-Genome Analysis of the Methyl tert-Butyl Ether-Degrading Beta-Proteobacterium Methylibium petroleiphilum PM1. J. Bacteriol.
189: 1931-1945
[Abstract]
[Full Text]
-
Chain, P. S. G., Denef, V. J., Konstantinidis, K. T., Vergez, L. M., Agullo, L., Reyes, V. L., Hauser, L., Cordova, M., Gomez, L., Gonzalez, M., Land, M., Lao, V., Larimer, F., LiPuma, J. J., Mahenthiralingam, E., Malfatti, S. A., Marx, C. J., Parnell, J. J., Ramette, A., Richardson, P., Seeger, M., Smith, D., Spilker, T., Sul, W. J., Tsoi, T. V., Ulrich, L. E., Zhulin, I. B., Tiedje, J. M.
(2006). Inaugural Article: Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc. Natl. Acad. Sci. USA
103: 15280-15287
[Abstract]
[Full Text]
-
Klotz, M. G., Arp, D. J., Chain, P. S. G., El-Sheikh, A. F., Hauser, L. J., Hommes, N. G., Larimer, F. W., Malfatti, S. A., Norton, J. M., Poret-Peterson, A. T., Vergez, L. M., Ward, B. B.
(2006). Complete Genome Sequence of the Marine, Chemolithoautotrophic, Ammonia-Oxidizing Bacterium Nitrosococcus oceani ATCC 19707. Appl. Environ. Microbiol.
72: 6299-6315
[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]
-
Cho, C. M.-H., Yan, T., Liu, X., Wu, L., Zhou, J., Stein, L. Y.
(2006). Transcriptome of a Nitrosomonas europaea Mutant with a Disrupted Nitrite Reductase Gene (nirK).. Appl. Environ. Microbiol.
72: 4450-4454
[Abstract]
[Full Text]
-
Mavromatis, K., Doyle, C. K., Lykidis, A., Ivanova, N., Francino, M. P., Chain, P., Shin, M., Malfatti, S., Larimer, F., Copeland, A., Detter, J. C., Land, M., Richardson, P. M., Yu, X. J., Walker, D. H., McBride, J. W., Kyrpides, N. C.
(2006). The Genome of the Obligately Intracellular Bacterium Ehrlichia canis Reveals Themes of Complex Membrane Structure and Immune Evasion Strategies. J. Bacteriol.
188: 4015-4023
[Abstract]
[Full Text]
-
Chain, P. S. G., Hu, P., Malfatti, S. A., Radnedge, L., Larimer, F., Vergez, L. M., Worsham, P., Chu, M. C., Andersen, G. L.
(2006). Complete Genome Sequence of Yersinia pestis Strains Antiqua and Nepal516: Evidence of Gene Reduction in an Emerging Pathogen.. J. Bacteriol.
188: 4453-4463
[Abstract]
[Full Text]
-
Starkenburg, S. R., Chain, P. S. G., Sayavedra-Soto, L. A., Hauser, L., Land, M. L., Larimer, F. W., Malfatti, S. A., Klotz, M. G., Bottomley, P. J., Arp, D. J., Hickey, W. J.
(2006). Genome Sequence of the Chemolithoautotrophic Nitrite-Oxidizing Bacterium Nitrobacter winogradskyi Nb-255.. Appl. Environ. Microbiol.
72: 2050-2063
[Abstract]
[Full Text]
-
Beller, H. R., Chain, P. S. G., Letain, T. E., Chakicherla, A., Larimer, F. W., Richardson, P. M., Coleman, M. A., Wood, A. P., Kelly, D. P.
(2006). The Genome Sequence of the Obligately Chemolithoautotrophic, Facultatively Anaerobic Bacterium Thiobacillus denitrificans. J. Bacteriol.
188: 1473-1488
[Abstract]
[Full Text]
-
Hommes, N. G., Kurth, E. G., Sayavedra-Soto, L. A., Arp, D. J.
(2006). Disruption of sucA, Which Encodes the E1 Subunit of {alpha}-Ketoglutarate Dehydrogenase, Affects the Survival of Nitrosomonas europaea in Stationary Phase. J. Bacteriol.
188: 343-347
[Abstract]
[Full Text]
-
Chain, P. S. G., Comerci, D. J., Tolmasky, M. E., Larimer, F. W., Malfatti, S. A., Vergez, L. M., Aguero, F., Land, M. L., Ugalde, R. A., Garcia, E.
(2005). Whole-Genome Analyses of Speciation Events in Pathogenic Brucellae. Infect. Immun.
73: 8353-8361
[Abstract]
[Full Text]
-
Huang, C.-H., Peng, J.
(2005). Evolutionary conservation and diversification of Rh family genes and proteins. Proc. Natl. Acad. Sci. USA
102: 15512-15517
[Abstract]
[Full Text]
-
Beaumont, H. J. E., Lens, S. I., Westerhoff, H. V., van Spanning, R. J. M.
(2005). Novel nirK Cluster Genes in Nitrosomonas europaea Are Required for NirK-Dependent Tolerance to Nitrite. J. Bacteriol.
187: 6849-6851
[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]
-
Urban, T. A., Goldberg, J. B., Forstner, J. F., Sajjan, U. S.
(2005). Cable Pili and the 22-Kilodalton Adhesin Are Required for Burkholderia cenocepacia Binding to and Transmigration across the Squamous Epithelium. Infect. Immun.
73: 5426-5437
[Abstract]
[Full Text]
-
Dobrinski, K. P., Longo, D. L., Scott, K. M.
(2005). The Carbon-Concentrating Mechanism of the Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena. J. Bacteriol.
187: 5761-5766
[Full Text]
-
Feil, H., Feil, W. S., Chain, P., Larimer, F., DiBartolo, G., Copeland, A., Lykidis, A., Trong, S., Nolan, M., Goltsman, E., Thiel, J., Malfatti, S., Loper, J. E., Lapidus, A., Detter, J. C., Land, M., Richardson, P. M., Kyrpides, N. C., Ivanova, N., Lindow, S. E.
(2005). Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc. Natl. Acad. Sci. USA
102: 11064-11069
[Abstract]
[Full Text]
-
Burton, E. O., Read, H. W., Pellitteri, M. C., Hickey, W. J.
(2005). Identification of Acyl-Homoserine Lactone Signal Molecules Produced by Nitrosomonas europaea Strain Schmidt. Appl. Environ. Microbiol.
71: 4906-4909
[Abstract]
[Full Text]
-
Shen, S., Mascarenhas, M., Morgan, R., Rahn, K., Karmali, M. A.
(2005). Identification of Four Fimbria-Encoding Genomic Islands That Are Highly Specific for Verocytotoxin-Producing Escherichia coli Serotype O157 Strains. J. Clin. Microbiol.
43: 3840-3850
[Abstract]
[Full Text]
-
Dedysh, S. N., Knief, C., Dunfield, P. F.
(2005). Methylocella Species Are Facultatively Methanotrophic. J. Bacteriol.
187: 4665-4670
[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]
-
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]
-
Schmidt, I., van Spanning, R. J. M., Jetten, M. S. M.
(2004). Denitrification and ammonia oxidation by Nitrosomonas europaea wild-type, and NirK- and NorB-deficient mutants. Microbiology
150: 4107-4114
[Abstract]
[Full Text]
-
Chain, P. S. G., Carniel, E., Larimer, F. W., Lamerdin, J., Stoutland, P. O., Regala, W. M., Georgescu, A. M., Vergez, L. M., Land, M. L., Motin, V. L., Brubaker, R. R., Fowler, J., Hinnebusch, J., Marceau, M., Medigue, C., Simonet, M., Chenal-Francisque, V., Souza, B., Dacheux, D., Elliott, J. M., Derbise, A., Hauser, L. J., Garcia, E.
(2004). Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA
101: 13826-13831
[Abstract]
[Full Text]
-
Franklin, M. J., Douthit, S. A., McClure, M. A.
(2004). Evidence that the algI/algJ Gene Cassette, Required for O Acetylation of Pseudomonas aeruginosa Alginate, Evolved by Lateral Gene Transfer. J. Bacteriol.
186: 4759-4773
[Abstract]
[Full Text]
-
Beaumont, H. J. E., van Schooten, B., Lens, S. I., Westerhoff, H. V., van Spanning, R. J. M.
(2004). Nitrosomonas europaea Expresses a Nitric Oxide Reductase during Nitrification. J. Bacteriol.
186: 4417-4421
[Abstract]
[Full Text]
-
Tian, M., Huitema, E., da Cunha, L., Torto-Alalibo, T., Kamoun, S.
(2004). A Kazal-like Extracellular Serine Protease Inhibitor from Phytophthora infestans Targets the Tomato Pathogenesis-related Protease P69B. J. Biol. Chem.
279: 26370-26377
[Abstract]
[Full Text]
-
Wei, X., Sayavedra-Soto, L. A., Arp, D. J.
(2004). The transcription of the cbb operon in Nitrosomonas europaea. Microbiology
150: 1869-1879
[Abstract]
[Full Text]
-
Schmidt, I., Steenbakkers, P. J. M., op den Camp, H. J. M., Schmidt, K., Jetten, M. S. M.
(2004). Physiologic and Proteomic Evidence for a Role of Nitric Oxide in Biofilm Formation by Nitrosomonas europaea and Other Ammonia Oxidizers. J. Bacteriol.
186: 2781-2788
[Abstract]
[Full Text]
-
Schmidt, I., Look, C., Bock, E., Jetten, M. S. M.
(2004). Ammonium and hydroxylamine uptake and accumulation in Nitrosomonas. Microbiology
150: 1405-1412
[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]
-
Okano, Y., Hristova, K. R., Leutenegger, C. M., Jackson, L. E., Denison, R. F., Gebreyesus, B., Lebauer, D., Scow, K. M.
(2004). Application of Real-Time PCR To Study Effects of Ammonium on Population Size of Ammonia-Oxidizing Bacteria in Soil. Appl. Environ. Microbiol.
70: 1008-1016
[Abstract]
[Full Text]
-
Hommes, N. G., Sayavedra-Soto, L. A., Arp, D. J.
(2003). Chemolithoorganotrophic Growth of Nitrosomonas europaea on Fructose. J. Bacteriol.
185: 6809-6814
[Abstract]
[Full Text]
-
Ramos, J.-L.
(2003). Lessons from the Genome of a Lithoautotroph: Making Biomass from Almost Nothing. J. Bacteriol.
185: 2690-2691
[Full Text]
Copyright © 2003 by the American Society for Microbiology. All rights reserved.