Abstract
Anaerobic ammonium oxidation (anammox) has become a main focus in oceanography and wastewater treatment1,2. It is also the nitrogen cycle's major remaining biochemical enigma. Among its features, the occurrence of hydrazine as a free intermediate of catabolism3,4, the biosynthesis of ladderane lipids5,6 and the role of cytoplasm differentiation7 are unique in biology. Here we use environmental genomics8,9—the reconstruction of genomic data directly from the environment—to assemble the genome of the uncultured anammox bacterium Kuenenia stuttgartiensis10 from a complex bioreactor community. The genome data illuminate the evolutionary history of the Planctomycetes and allow us to expose the genetic blueprint of the organism's special properties. Most significantly, we identified candidate genes responsible for ladderane biosynthesis and biological hydrazine metabolism, and discovered unexpected metabolic versatility.
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References
Arrigo, R. A. Marine microorganisms and global nutrient cycles. Nature 437, 349–355 (2005)
Strous, M. & Jetten, M. S. M. Anaerobic oxidation of methane and ammonium. Annu. Rev. Microbiol. 58, 99–117 (2004)
Van de Graaf, A. A., De Bruijn, P., Robertson, L. A., Jetten, M. S. M. & Kuenen, J. G. Metabolic pathway of anaerobic ammonium oxidation on the basis of N-15 studies in a fluidized bed reactor. Microbiology (UK) 143, 2415–2421 (1997)
Schalk, J., de Vries, S., Kuenen, J. G. & Jetten, M. S. M. A novel hydroxylamine oxidoreductase involved in the anammox process. Biochemistry 39, 5405–5412 (2000)
Sinninghe Damsté, J. S. et al. Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419, 708–712 (2002)
Macitti, V. & Corey, E. J. Total synthesis of pentacyclic anammoxic acid. J. Am. Chem. Soc. 126, 15664–15665 (2004)
Lindsay, M. R. et al. Cell compartmentalization in planctomycetes: novel types of structural organization for the bacterial cell. Arch. Microbiol. 175, 413–429 (2001)
DeLong, E. F. Microbial community genomics in the ocean. Nature Rev. Microbiol. 3, 459–469 (2005)
Tringe, S. G. et al. Comparative metagenomics of microbial communities. Science 308, 554–557 (2005)
Schmid, M. C. et al. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst. Appl. Microbiol. 23, 93–106 (2000)
Von Mering, C. et al. STRING: known and predicted protein–protein associations, integrated and transferred across organisms. Nucleic Acids Res. 33, D433–D437 (2005)
Methe, B. A. et al. Genome of Geobacter sulfurreducens: Metal reduction in subsurface environments. Science 302, 1967–1969 (2003)
Heidelberg, J. F. et al. Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nature Biotechnol. 20, 1118–1123 (2002)
Chain, P. et al. Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J. Bacteriol. 185, 2759–2773 (2003)
Brasseura, G. et al. Apparent redundancy of electron transfer pathways via bc1 complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans. Biochim. Biophys. Acta 1656, 114–126 (2004)
Güven, D. et al. Propionate oxidation by and methanol inhibition of anaerobic ammonium-oxidizing bacteria. Appl. Environ. Microbiol. 71, 1066–1071 (2005)
Schouten, S. et al. Stable carbon isotopic fractionations associated with inorganic carbon fixation by anaerobic ammonium oxidizing bacteria. Appl. Environ. Microbiol. 40, 3785–3788 (2004)
Drake, H. L. & Daniel, S. L. Physiology of the thermophilic acetogen Moorella thermoacetica. Res. Microbiol. 155, 422–436 (2004)
Layer, G., Heinz, D. W., Jahn, D. & Schubert, W. D. Structure and function of radical SAM enzymes. Curr. Opin. Chem. Biol. 8, 468–476 (2004)
Brochier, C. & Philippe, H. Phylogeny—A non hyperthermophilic ancestor for bacteria. Nature 417, 244 (2002)
Fuerst, J. A. Intracellular compartmentation in planctomycetes. Annu. Rev. Microbiol. 59, 299–328 (2005)
Teeling, H., Lombardot, T., Bauer, M., Ludwig, W. & Glöckner, F. O. Evaluation of the phylogenetic position of the planctomycete ‘Rhodopirellula baltica’ SH 1 by means of concatenated ribosomal protein sequences, DNA-directed RNA polymerase subunit sequences and whole genome trees. Int. J. Syst. Evol. Microbiol. 54, 791–801 (2004)
Chopra, I., Storey, C., Falla, T. J. & Pearce, J. H. Antibiotics, peptidoglycan synthesis and genomics: the chlamydial anomaly revisited. Microbiology (UK) 144, 2673–2678 (1998)
Glöckner, F. O. et al. Complete genome sequence of the marine planctomycete Pirellula sp. Strain 1. Proc. Natl Acad. Sci. USA 100, 8298–8303 (2003)
Staley, J. T., Bouzek, H. & Jenkins, C. Eukaryotic signature proteins of Prosthecobacter dejongeii and Gemmata sp Wa-1 as revealed by in silico analysis. FEMS Microbiol. Lett. 243, 9–14 (2005)
Daims, H., Lücker, S. & Wagner, M. DAIME, a novel image analysis program for microbial ecology and biofilm research. Environ. Microbiol. 8, 200–213 (2006)
Le Paslier, M. C. et al. Construction and characterization of a Schistosoma mansoni bacterial artificial chromosome library. Genomics 65, 87–94 (2000)
Frishman, D. et al. Functional and structural genomics using PEDANT. Bioinformatics 17, 44–57 (2001)
Vishwanath, P., Favaretto, P., Hartman, H., Mohr, S. C. & Smith, T. F. Ribosomal protein-sequence block structure suggests complex prokaryotic evolution with implications for the origin of eukaryotes. Mol. Phylogenet. Evol. 33, 615–625 (2004)
Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)
Acknowledgements
Preliminary sequence data from G. obscuriglobus was obtained from The Institute for Genomic Research through the website at http://www.tigr.org. Sequencing of G. obscuriglobus was accomplished with support from the United States Department of Energy. A. Cabezas is acknowledged for technical assistance. M.H., A.C. and M.W. were supported by the Austrian Ministry for Science and Education. M.T. was funded by the German Federal Ministry for Education and Research (Biolog II). H.D. was supported by the Wiener Wissenschafts-, Forschungs- und Technologiefonds (WWTF). We thank B. Anneser, F. Maixner, M. Leitner, A. Pol and B. Meijerink for help in the first round annotation and M. Ott for his effort in high performance phylogenetic treeing. The Dutch anammox research was supported by the Netherlands Science Foundation for Earth and Life Science (ALW), the Foundation for Applied Research (STW) and the European Union. The Radboud University and S. Wendelaar Bonga financially supported the initial phase of the project.
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Supplementary information
Supplementary Figure legends
(DOC 27 kb)
Supplementary Methods
(PDF 127 kb)
Supplementary Figure 1
Maximum-likelihood tree displaying the16S rRNA gene diversity in the anammox enrichment culture from which the K. stuttgartiensis genome was reconstructed. (PDF 57 kb)
Supplementary Figure 2
Representation of the K. stuttgartiensis chromosome including annotated coding sequences and RNA genes. (PDF 425 kb)
Supplementary Figure 3
Functional redundancy in catabolism and respiration in K. stuttgartiensis compared to other bacteria. (PDF 130 kb)
Supplementary Figure 4
Phylogenetic consensus tree based on concatenated 5S-16S-23S rRNA sequences, showing the phylogenetic positioning of K. stuttgartiensis within the Bacteria. (PDF 15 kb)
Supplementary Figure 5
Distance (FITCH with the Dayhoff-PAM model), maximum parsimony (MP) and maximum likelihood (PHYML with the Dayhoff-PAM model) phylogenetic trees based on 26 concatenated ribosomal protein sequences (see Supplementary Methods), showing the phylogenetic positioning of K. stuttgartiensis within the Bacteria. (PDF 25 kb)
Supplementary Table 1
General features of the Kuenenia stuttgartiensis genome and comparison with Rhodopirellula baltica. (PDF 16 kb)
Supplementary Table 2
Genes with known homologues involved in respiration. (PDF 24 kb)
Supplementary Table 3
Iron and manganese respiration by the anammox bacterium Kuenenia stuttgartiensis. (PDF 82 kb)
Supplementary Table 4
Genes with known homologues involved in carbon metabolism. (PDF 16 kb)
Supplementary Table 5
CO2 fixation pathway in Kuenenia stuttgartiensis. (PDF 29 kb)
Supplementary Table 6
Proteins (gene names) used for phylogenetic analysis. (PDF 18 kb)
Supplementary Table 7
List of orthologous groups (OG) in which both Chlamydiae and Planctomycetes are heavily represented, to the exclusion of most other sequenced bacteria. (PDF 39 kb)
Supplementary Table 8
Genes with homologues involved in peptidoglycan biosynthesis and cell division. (PDF 12 kb)
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Strous, M., Pelletier, E., Mangenot, S. et al. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790–794 (2006). https://doi.org/10.1038/nature04647
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DOI: https://doi.org/10.1038/nature04647
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