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J Bacteriol. Oct 2011; 193(19): 5539–5540.
PMCID: PMC3187385

Genome Sequence of an Ammonia-Oxidizing Soil Archaeon, “Candidatus Nitrosoarchaeum koreensis” MY1

Abstract

Ammonia-oxidizing archaea are ubiquitous microorganisms which play important roles in global nitrogen and carbon cycle on earth. Here we present the high-quality draft genome sequence of an ammonia-oxidizing archaeon, “Candidatus Nitrosopumilus koreensis” MY1, that dominated an enrichment culture of a soil sample from the rhizosphere. Its genome contains genes for survival in the rhizosphere environment as well as those for carbon fixation and ammonium oxidation to nitrite.

GENOME ANNOUNCEMENT

Ammonia-oxidizing archaea belonging to the archaeal phylum Thaumarchaeota are ubiquitous microbes in marine, freshwater, and terrestrial environments (1, 4, 13, 18, 19, 24). They are capable of using ammonia oxidation as an energy source in nutrient-deprived oligotrophic environments and performing carbon fixation through the 3-hydroxypropionate/4-hydroxybutryrate pathway (2, 9, 16, 20, 25). Particularly, increased nitrification in the rhizosphere is reportedly due to ammonia-oxidizing archaea (5, 10).

Despite these significant contributions to the global carbon and nitrogen cycle, many questions about the physiology, metabolism, and ecological niches of the mesophilic ammonia-oxidizing archaea remain unanswered owing to the difficulty of isolation. Only a single species, Nitrosopumilus maritimus SCM1, has been isolated from a tropical marine aquarium (15), and no strain in the rhizosphere has been cultured and analyzed.

Candidatus Nitrosoarchaeum koreensis” MY1 dominated an enrichment culture of a soil sample from the rhizosphere of Caragana sinica (M.-Y. Jung. et al., submitted for publication). The 16S rRNA gene sequence from MY1 is most closely related to that of “Candidatus Nitrosoarchaeum limnia” SFB1 from low-salinity sediments. The genome sequence of MY1 was determined by next generation sequencing technologies.

Paired-end sequences of 2.2 Gb (~1,376-fold genome coverage) were produced from 600-bp and 3-kb genomic libraries with Illumina/Solexa Genome Analyzer IIx (DNA Link, Inc.), and 223.5-Mb single-ended sequences (~139-fold genome coverage) were produced with Roche/454 Genome Sequencer FLX Titanium. Assembly and contig editing were performed with CLC Genomics Workbench (CLC bio, Inc.) and Phred/Phrap/Consed. A total of 1,945 coding sequences (89.4% coding density) were predicted by Glimmer 3.02 and annotated using the information from GenBank, UniProt, COG, KEGG, Pfam, and RAST (21).

The final assembly consists of a single contig of 1,607,695 bp (32.7% G+C content). The genomes of MY1, SFB1, and SCM1 display a very high degree of synteny. A total of 1,317 protein-coding genes (67.1%) were assigned predicted functions. The genome has one 16S-23S rRNA operon, a distantly located 5S rRNA gene, and 42 tRNA genes. No transposase gene or CRISPR locus was detected. Most of the MY1-specific genes are of unknown functions.

The genome contains genes coding for an ammonia monooxygenase complex and an ammonium transporter for ammonium oxidation, nitrite reductases for ammonium assimilation or NO formation, and a nitric oxide oxidoreductase for denitrification, but like other ammonia-oxidizing archaea, no hydroxylamine oxidase gene was detected (3, 8, 23). MY1 also has an almost complete set of genes of the modified 3-hydroxypropionate/4-hydroxybutryrate pathway for carbon fixation and phosphoenolpyruvate carboxykinase and fructose-1,6-bisphosphatase for gluconeogenesis, though malonate semialdehyde reductase was not detected (2, 6, 8).

Unlike ammonia-oxidizing archaea from the ocean, MY1 is thought to have a citrate transporter for citrate utilization and NiFe-hydrogenase genes related to energy metabolism to survive competition in the rhizosphere (12, 22). Also, instead of genes coding for the ectoine biosynthesis pathway to tolerate salt stress (7, 14), MY1 keeps a number of genes to cope with oxidative stress and antibiotic resistance genes (17).

Nucleotide sequence accession number.

The draft genome sequence of “Candidatus Nitrosoarchaeum koreensis” MY1 has been deposited in GenBank under accession no. AFPU00000000. The sequence and annotation are also available from the Genome Encyclopedia of Microbes (GEM; http://www.gem.re.kr) (11).

Acknowledgments

We thank Haeyoung Jeong, Hong-Seog Park, Sang-Haeng Choi, and members of GEM and the KRIBB sequencing team for technical support.

This work was supported by the 21C Frontier Microbial Genomics and Applications Center Program of the Ministry of Education, Science and Technology, Republic of Korea.

REFERENCES

1. Auguet J. C., Nomokonova N., Camarero L., Casamayor E. O. 2011. Seasonal changes of freshwater ammonia-oxidizing archaeal assemblages and nitrogen species in oligotrophic alpine lakes. Appl. Environ. Microbiol. 77:1937–1945 [PMC free article] [PubMed]
2. Berg I. A., Kockelkorn D., Buckel W., Fuchs G. 2007. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318:1782–1786 [PubMed]
3. Blainey P. C., Mosier A. C., Potanina A., Francis C. A., Quake S. R. 2011. Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 6:e16626. [PMC free article] [PubMed]
4. Brochier-Armanet C., Boussau B., Gribaldo S., Forterre P. 2008. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6:245–252 [PubMed]
5. Chen X. P., Zhu Y. G., Xia Y., Shen J. P., He J. Z. 2008. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ. Microbiol. 10:1978–1987 [PubMed]
6. Chuakrut S., Arai H., Ishii M., Igarashi Y. 2003. Characterization of a bifunctional archaeal acyl coenzyme A carboxylase. J. Bacteriol. 185:938–947 [PMC free article] [PubMed]
7. Goller K., Ofer A., Galinski E. A. 1998. Construction and characterization of an NaCl-sensitive mutant of Halomonas elongata impaired in ectoine biosynthesis. FEMS Microbiol. Lett. 161:293–300 [PubMed]
8. Hallam S. J., et al. 2006. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl. Acad. Sci. U. S. A. 103:18296–18301 [PMC free article] [PubMed]
9. Hallam S. J., et al. 2006. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol. 4:e95. [PMC free article] [PubMed]
10. Herrmann M., Saunders A. M., Schramm A. 2008. Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl. Environ. Microbiol. 74:3279–3283 [PMC free article] [PubMed]
11. Jeong H., Yoon S. H., Yu D. S., Oh T. K., Kim J. F. 2008. Recent progress of microbial genome projects in Korea. Biotechnol. J. 3:601–611 [PubMed]
12. Kamilova F., et al. 2006. Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol. Plant Microbe Interact. 19:250–256 [PubMed]
13. Karner M. B., DeLong E. F., Karl D. M. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510 [PubMed]
14. Kol S., et al. 2010. Metabolomic characterization of the salt stress response in Streptomyces coelicolor. Appl. Environ. Microbiol. 76:2574–2581 [PMC free article] [PubMed]
15. Konneke M., et al. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546 [PubMed]
16. Martens-Habbena W., Berube P. M., Urakawa H., de la Torre J. R., Stahl D. A. 2009. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461:976–979 [PubMed]
17. Matilla M. A., Espinosa-Urgel M., Rodriguez-Herva J. J., Ramos J. L., Ramos-Gonzalez M. I. 2007. Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol. 8:R179. [PMC free article] [PubMed]
18. Ochsenreiter T., Selezi D., Quaiser A., Bonch-Osmolovskaya L., Schleper C. 2003. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ. Microbiol. 5:787–797 [PubMed]
19. Park B. J., et al. 2010. Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria. Appl. Environ. Microbiol. 76:7575–7587 [PMC free article] [PubMed]
20. Pratscher J., Dumont M. G., Conrad R. 2011. Ammonia oxidation coupled to CO2 fixation by archaea and bacteria in an agricultural soil. Proc. Natl. Acad. Sci. U. S. A. 108:4170–4175 [PMC free article] [PubMed]
21. Song J. Y., et al. 2010. Draft genome sequence of Streptomyces clavuligerus NRRL 3585, a producer of diverse secondary metabolites. J. Bacteriol. 192:6317–6318 [PMC free article] [PubMed]
22. Vignais P. M., Colbeau A. 2004. Molecular biology of microbial hydrogenases. Curr. Issues Mol. Biol. 6:159–188 [PubMed]
23. Walker C. B., et al. 2010. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. U. S. A. 107:8818–8823 [PMC free article] [PubMed]
24. Wuchter C., et al. 2006. Archaeal nitrification in the ocean. Proc. Natl. Acad. Sci. U. S. A. 103:12317–12322 [PMC free article] [PubMed]
25. Wuchter C., Schouten S., Boschker H. T., Sinninghe Damste J. S. 2003. Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol. Lett. 219:203–207 [PubMed]

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