Cyanate as an energy source for nitrifiers

Nature

Volumn 524, Issue 7563, 2015, Pages 105-108

  Palatinszky, Marton ^a   Herbold, Craig ^a   Jehmlich, Nico ^a   Pogoda, Mario ^b   Han, Ping ^a   Von Bergen, Martin ^a   Lagkouvardos, Ilias ^b,c,d   Karst, Søren M ^a   Galushko, Alexander ^c,e   Koch, Hanna ^a   Berry, David ^a   Daims, Holger ^a   Wagner, Michael ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^c AALBORG UNIVERSITY   (Denmark)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e AGROPHYSICAL RESEARCH INSTITUTE   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; CARBON DIOXIDE; CYANASE; CYANIC ACID; LYASE; UNCLASSIFIED DRUG; AMMONIUM DERIVATIVE; CYANATE HYDROLASE; CYANIC ACID DERIVATIVE; NITRIC ACID DERIVATIVE; NITRITE; NITROGEN;

AMMONIA; AMMONIUM; BIOTECHNOLOGY; CARBON DIOXIDE; CLADISTICS; ENERGY EFFICIENCY; ENZYME ACTIVITY; GENOME; GROWTH RATE; METABOLISM; MICROORGANISM; NITRIFICATION; NITRIFYING BACTERIUM; NITROGEN COMPOUND; NITROGEN CYCLE; OXIC CONDITIONS; TERRESTRIAL ECOSYSTEM; UREA;

AMMONIA OXIDIZER; AMMONIA OXIDIZING ARCHAEON; AQUATIC ENVIRONMENT; ARTICLE; CONTROLLED STUDY; ENERGY RESOURCE; METAGENOME; MICROBIAL GROWTH; MULTIGENE FAMILY; NITRIFYER; NITRITE OXIDIZER; NITROGEN CYCLING; NITROSOSPHAERA GARGENSIS; NONHUMAN; PRIORITY JOURNAL; THAUMARCHAEOTA; AEROBIC METABOLISM; ARCHAEON; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; NITRIFICATION; NITROGEN CYCLE; OXIDATION REDUCTION REACTION;

BACTERIA (MICROORGANISMS); NITROSOMONADALES; NITROSPIRA;

AEROBIOSIS; AMMONIA; AMMONIUM COMPOUNDS; ARCHAEA; CARBON DIOXIDE; CARBON-NITROGEN LYASES; CYANATES; ENVIRONMENTAL MICROBIOLOGY; METAGENOME; NITRATES; NITRIFICATION; NITRITES; NITROGEN; NITROGEN CYCLE; OXIDATION-REDUCTION;

EID: 84938798019     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14856     Document Type: Article

References (47)

1. Hatzenpichler, R. et al. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl Acad. Sci. USA 105, 2134-2139 (2008).
2. Kamennaya, N. A. & Post, A. F. Distribution and expression of the cyanate acquisition potential among cyanobacterial populations in oligotrophic marine waters. Limnol. Oceanogr. 58, 1959-1971 (2013).
3. Qian, M., Eaton, J. W. & Wolff, S. P. Cyanate-mediated inhibition of neutrophil myeloperoxidase activity. Biochem. J. 326, 159-166 (1997).
4. Purcarea, C. et al. Aquifex aeolicus aspartate transcarbamoylase, an enzyme specialized for the efficient utilization of unstable carbamoyl phosphate at elevated temperature. J. Biol. Chem. 278, 52924-52934 (2003).
5. Ubalua, A. O. Cyanogenic glycosides and the fate of cyanide in soil. Aust. J. Crop. Sci. 4, 223-237 (2010).
6. Widner, B., Mulholland, M. R. & Mopper, K. Chromatographic determination of nanomolar cyanate concentrations in estuarine and sea waters by precolumn fluorescence derivatization. Anal. Chem. 85, 6661-6666 (2013).
7. Rees, A. P., Woodward, E. M. S. & Joint, I. Concentrations and uptake of nitrate and ammonium in the Atlantic Ocean between 60 degrees N and 50 degrees S. Deep Sea Res. II 53, 1649-1665 (2006).
8. Rocap, G. et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042-1047 (2003).
9. Luque-Almagro, V. M. et al. Characterization of the Pseudomonas pseudoalcaligenes CECT5344 cyanase, an enzyme that is not essential for cyanide assimilation. Appl. Environ. Microbiol. 74, 6280-6288 (2008).
10. Kamennaya, N. A., Chernihovsky, M.& Post, A. F. The cyanate utilization capacity of marine unicellular Cyanobacteria. Limnol. Oceanogr. 53, 2485-2494 (2008).
11. Bock, E. Growth of nitrobacter in the presence of organic matter. II. Chemoorganotrophic growth of Nitrobacter agilis. Arch. Microbiol. 108, 305-312 (1976).
12. Bock, E., Schmidt, I., Stuven, R. & Zart, D. Nitrogen loss caused by denitrifying Nitrosomonas cells using ammonium or hydrogen as electron-donors and nitrite as electron-acceptor. Arch. Microbiol. 163, 16-20 (1995).
13. Hommes, N. G., Sayavedra-Soto, L. A.&Arp, D. J. Chemolithoorganotrophic growth of Nitrosomonas europaea on fructose. J. Bacteriol. 185, 6809-6814 (2003).
14. Mussmann, M. et al. Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc. Natl Acad. Sci. USA 108, 16771-16776 (2011).
15. Koch, H. et al. Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science 345, 1052-1054 (2014).
16. Tourna, M. et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl Acad. Sci. USA 108, 8420-8425 (2011).
17. Qin, W. et al. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc. Natl Acad. Sci. USA 111, 12504-12509 (2014).
18. Spang, A. et al. The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ. Microbiol. 14, 3122-3145 (2012).
19. Stieglmeier, M. et al. Nitrososphaera viennensis gen. nov., sp nov., an aerobic and mesophilic, ammonia-oxidizing archaeon fromsoil and amember of the archaeal phylum Thaumarchaeota. Int. J. Syst. Evol. Microbiol. 64, 2738-2752 (2014).
20. Maeda, S.&Omata, T. Nitrite transport activity of the ABC-type cyanate transporter of the cyanobacterium Synechococcus elongatus. J. Bacteriol. 191, 3265-3272 (2009).
21. Munoz-Centeno. M. C., Paneque, A. & Cejudo, F. J. Cyanate is transported by the nitrate permease in Azotobacter chroococcum. FEMS Microbiol. Lett. 137, 91-94 (1996).
22. Schramm, A., de Beer, D., van den Heuvel, J. C., Ottengraf, S. & Amann, R. Microscale distribution of populations and activities of Nitrosospira and Nitrospira spp. along a macroscale gradient in a nitrifying bioreactor: Quantification by in situ hybridization and the use of microsensors. Appl. Environ. Microbiol. 65, 3690-3696 (1999).
23. Maixner, F. et al. Nitrite concentration influences the population structure of Nitrospira-like bacteria. Environ. Microbiol. 8, 1487-1495 (2006).
24. Koops, H. P., Bottcher, B., Moller, U. C., Pommereningroser, A. & Stehr, G. Classification of eight new species of ammonia-oxidizing bacteria: Nitrosomonas communis sp. nov., Nitrosomonas ureae sp. nov., Nitrosomonas aestuarii sp. nov., Nitrosomonas marina sp. nov., Nitrosomonas nitrosa sp. nov., Nitrosomonas eutropha sp. nov., Nitrosomonas oligotropha sp. nov. and Nitrosomonas halophila sp. nov. J. Gen. Microbiol. 137, 1689-1699 (1991).
25. Markowitz, V. M. et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 42, D560-D567 (2014).
26. Daims, H., Nielsen, J. L., Nielsen, P. H., Schleifer, K. H. & Wagner, M. In situ characterization of Nitrospira-like nitrite oxidizing bacteria active in wastewater treatment plants. Appl. Environ. Microbiol. 67, 5273-5284 (2001).
27. Alonso-Sáez, L. et al. Role for urea in nitrification by polar marine Archaea. Proc. Natl Acad. Sci. USA 109, 17989-17994 (2012).
28. Suchard, M. A. & Redelings, B. D. BAli-Phy: simultaneous Bayesian inference of alignment and phylogeny. Bioinformatics 22, 2047-2048 (2006).
29. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
30. Lebedeva, E. V. et al. Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon Ca. Nitrosotenuis uzonensis representing a clade globally distributed in thermal habitats. PLoS ONE 8, e80835 (2013).
31. Widdel, F. Anaerober Abbau von Fettsaüren und Benzoesaüre durch neu isolierte Arten Sulfat-reduzierender Bakterien. Dissertation, Universität Göttingen (1980).
32. Ehrich, S., Behrens, D., Lebedeva, E., Ludwig, W. & Bock, E. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch. Microbiol. 164, 16-23 (1995).
33. Strickland, J. D. H. & Parsons, T. R. A Practical Handbook of Seawater Analysis. (Fisheries Research Board of Canada, 1972).
34. Kandeler, E.&Gerber, H. Short-termassay of soil urease activity using colorimetric determination of ammonium. Biol. Fertil. Soils 6, 68-72 (1988).
35. Guilloton, M. & Karst, F. A spectrophotometric determination of cyanate using reaction with 2-aminobenzoic acid. Anal. Biochem. 149, 291-295 (1985).
36. Mobarry, B. K., Wagner, M., Urbain, V., Rittmann, B. E. & Stahl, D. A. Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Appl. Environ. Microbiol. 62, 2156-2162 (1996).
37. Schiffmann, C. L. et al. Proteome profile and proteogenomics of the organohaliderespiring bacterium Dehalococcoides mccartyi strain CBDB1 grown on hexachlorobenzene as electron acceptor. J. Proteomics 98, 59-64 (2014).
38. Käll, L., Canterbury, J.D., Weston, J., Noble, W. S.& MacCoss, M. J. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nature Methods 4, 923-925 (2007).
39. Gallant, R. Nonlinear Equation Estimation 610 (John Wiley and Sons, 1987).
40. Henningsen, A. & Hamann, J. D. systemfit: A package for estimating systems of simultaneous equations in R. J. Stat. Softw. 23, 1-40 (2007).
41. Team, R. D. C. R. A language and environment for statistical computing. Proc. Natl Acad. Sci. USA http://www.R-project.org/(2011).
42. DeMartini, N., Murzin, D. Y., Forssen, M. & Hupa, M. Kinetics of cyanate decomposition in alkaline solutions of high ionic strength: The catalytic effect of bicarbonate. Ind. Eng. Chem. Res. 43, 4815-4821 (2004).
43. Taillades, J. et al. A pH-dependent cyanate reactivity model: application to preparative N-carbamoylation of amino acids. J. Chem. Soc. Perk. T. 2, 1247-1254 (2001).
44. UniProt Consortium.. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res. 42, D191-D198 (2014).
45. Katoh, K.& Standley, D.M.MAFFTmultiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780 (2013).
46. Altschul, S. F., Gish, W., Miller, W., Myers, E.W.&Lipman, D. J.Basic Local Alignment Search Tool. J. Mol. Biol. 215, 403-410 (1990).
47. Marchler-Bauer, A. et al. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 41, D348-D352 (2013).