1887

Abstract

Two mesophilic, neutrophilic and aerobic marine ammonia-oxidizing archaea, designated strains NF5 and D3C, were isolated from coastal surface water of the Northern Adriatic Sea. Cells were straight small rods 0.20–0.25 µm wide and 0.49–2.00 µm long. Strain NF5 possessed archaella as cell appendages. Glycerol dibiphytanyl glycerol tetraethers with zero to four cyclopentane moieties (GDGT-0 to GDGT-4) and crenarchaeol were the major core lipids. Menaquinone MK6 : 0 was the major respiratory quinone. Both isolates gained energy by oxidizing ammonia (NH3) to nitrite (NO2 ) and used bicarbonate as a carbon source. Strain D3C was able use urea as a source of ammonia for energy production and growth. Addition of hydrogen peroxide (H2O2) scavengers (catalase or α-keto acids) was required to sustain growth. Optimal growth occurred between 30 and 32 °C, pH 7.1 and 7.3 and between 34 and 37‰ salinity. The cellular metal abundance ranking of both strains was Fe>Zn>Cu>Mn>Co. The genomes of strains NF5 and D3C have a DNA G+C content of 33.4 and 33.8 mol%, respectively. Phylogenetic analyses of 16S rRNA gene sequences revealed that both strains are affiliated with the class Nitrososphaeria , sharing ~85 % 16S rRNA gene sequence identity with Nitrososphaera viennensis EN76. The two isolates are separated by phenotypic and genotypic characteristics and are assigned to distinct species within the genus Nitrosopumilus gen. nov. according to average nucleotide identity thresholds of their closed genomes. Isolates NF5 (=JCM 32270 =NCIMB 15114) and D3C (=JCM 32271 =DSM 106147 =NCIMB 15115) are type strains of the species Nitrosopumilus adriaticus sp. nov. and Nitrosopumilus piranensis sp. nov., respectively.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.003360
2019-04-02
2019-08-26
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/69/7/1892.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.003360&mimeType=html&fmt=ahah

References

  1. Wuchter C, Abbas B, Coolen MJ, Herfort L, van Bleijswijk J, van BJ et al. Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 2006;103:12317–12322 [CrossRef][PubMed]
    [Google Scholar]
  2. Leininger S, Urich T, Schloter M, Schwark L, Qi J et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 2006;442:806–809 [CrossRef][PubMed]
    [Google Scholar]
  3. Karner MB, Delong EF, Karl DM. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 2001;409:507–510 [CrossRef][PubMed]
    [Google Scholar]
  4. Teira E, Reinthaler T, Pernthaler A, Pernthaler J, Herndl GJ. Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by bacteria and Archaea in the deep ocean. Appl Environ Microbiol 2004;70:4411–4414 [CrossRef][PubMed]
    [Google Scholar]
  5. Wuchter C, Schouten S, Boschker HT, Sinninghe Damsté JS. Bicarbonate uptake by marine Crenarchaeota. FEMS Microbiol Lett 2003;219:203–207 [CrossRef][PubMed]
    [Google Scholar]
  6. Könneke M, Bernhard AE, de La Torre JR, Walker CB, Waterbury JB et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005;437:543–546 [CrossRef][PubMed]
    [Google Scholar]
  7. Ingalls AE, Shah SR, Hansman RL, Aluwihare LI, Santos GM et al. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon. Proc Natl Acad Sci USA 2006;103:6442–6447 [CrossRef][PubMed]
    [Google Scholar]
  8. Prosser JI, Nicol GW. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 2008;10:2931–2941 [CrossRef][PubMed]
    [Google Scholar]
  9. Martens-Habbena W, Berube PM, Urakawa H, de La Torre JR, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 2009;461:976–979 [CrossRef]
    [Google Scholar]
  10. Horak RE, Qin W, Schauer AJ, Armbrust EV, Ingalls AE et al. Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by archaea. ISME J 2013;7:2023–2033 [CrossRef][PubMed]
    [Google Scholar]
  11. Lam P, Kuypers MM. Microbial nitrogen cycling processes in oxygen minimum zones. Ann Rev Mar Sci 2011;3:317–345 [CrossRef][PubMed]
    [Google Scholar]
  12. Stewart FJ, Ulloa O, Delong EF. Microbial metatranscriptomics in a permanent marine oxygen minimum zone. Environ Microbiol 2012;14:23–40 [CrossRef][PubMed]
    [Google Scholar]
  13. Hawley AK, Brewer HM, Norbeck AD, Paša-Tolić L, Hallam SJ. Metaproteomics reveals differential modes of metabolic coupling among ubiquitous oxygen minimum zone microbes. Proc Natl Acad Sci USA 2014;111:11395–11400 [CrossRef][PubMed]
    [Google Scholar]
  14. Qin W, Meinhardt KA, Moffett JW, Devol AH, Virginia Armbrust E et al. Influence of oxygen availability on the activities of ammonia-oxidizing archaea. Environ Microbiol Rep 2017;9:250–256 [CrossRef][PubMed]
    [Google Scholar]
  15. Santoro AE, Buchwald C, McIlvin MR, Casciotti KL. Isotopic signature of N(2)O produced by marine ammonia-oxidizing archaea. Science 2011;333:1282–1285 [CrossRef][PubMed]
    [Google Scholar]
  16. Löscher CR, Kock A, Könneke M, Laroche J, Bange HW et al. Production of oceanic nitrous oxide by ammonia-oxidizing archaea. Biogeosciences 2012;9:2419–2429 [CrossRef]
    [Google Scholar]
  17. Freing A, Wallace DW, Bange HW. Global oceanic production of nitrous oxide. Philos Trans R Soc Lond B Biol Sci 2012;367:1245–1255 [CrossRef][PubMed]
    [Google Scholar]
  18. Qin W, Heal KR, Ramdasi R, Kobelt JN, Martens-Habbena W et al. Nitrosopumilus maritimus gen. nov., sp. nov., Nitrosopumilus cobalaminigenes sp. nov., Nitrosopumilus oxyclinae sp. nov., and Nitrosopumilus ureiphilus sp. nov., four marine ammonia-oxidizing archaea of the phylum Thaumarchaeota. Int J Syst Evol Microbiol 2017;67:5067–5079 [CrossRef][PubMed]
    [Google Scholar]
  19. Bayer B, Vojvoda J, Offre P, Alves RJ, Elisabeth NH et al. Physiological and genomic characterization of two novel marine thaumarchaeal strains indicates niche differentiation. ISME J 2016;10:1051–1063 [CrossRef][PubMed]
    [Google Scholar]
  20. Park SJ, Ghai R, Martín-Cuadrado AB, Rodríguez-Valera F, Chung WH et al. Genomes of two new ammonia-oxidizing archaea enriched from deep marine sediments. PLoS One 2014;9:e96449 [CrossRef][PubMed]
    [Google Scholar]
  21. Mosier AC, Allen EE, Kim M, Ferriera S, Francis CA. Genome sequence of "Candidatus Nitrosopumilus salaria" BD31, an ammonia-oxidizing archaeon from the San Francisco Bay Estuary. J Bacteriol 2012;194:2121–2122 [CrossRef][PubMed]
    [Google Scholar]
  22. Mosier AC, Lund MB, Francis CA. Ecophysiology of an ammonia-oxidizing archaeon adapted to low-salinity habitats. Microb Ecol 2012;64:955–963 [CrossRef][PubMed]
    [Google Scholar]
  23. Santoro AE, Dupont CL, Richter RA, Craig MT, Carini P et al. Genomic and proteomic characterization of "Candidatus Nitrosopelagicus brevis": an ammonia-oxidizing archaeon from the open ocean. Proc Natl Acad Sci USA 2015;112:1173–1178 [CrossRef][PubMed]
    [Google Scholar]
  24. Ahlgren NA, Chen Y, Needham DM, Parada AE, Sachdeva R et al. Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems. Environ Microbiol 2017;19:2434–2452 [CrossRef][PubMed]
    [Google Scholar]
  25. Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci USA 2011;108:8420–8425 [CrossRef][PubMed]
    [Google Scholar]
  26. Zhalnina KV, Dias R, Leonard MT, Dorr de Quadros P, Camargo FA et al. Genome sequence of Candidatus Nitrososphaera evergladensis from group I.1b enriched from Everglades soil reveals novel genomic features of the ammonia-oxidizing archaea. PLoS One 2014;9:e101648 [CrossRef][PubMed]
    [Google Scholar]
  27. Jung MY, Park SJ, Kim SJ, Kim JG, Sinninghe Damsté JS et al. A mesophilic, autotrophic, ammonia-oxidizing archaeon of thaumarchaeal group I.1a cultivated from a deep oligotrophic soil horizon. Appl Environ Microbiol 2014;80:3645–3655 [CrossRef][PubMed]
    [Google Scholar]
  28. Lehtovirta-Morley LE, Ross J, Hink L, Weber EB, Gubry-Rangin C et al. Isolation of ‘Candidatus Nitrosocosmicus franklandus’, a novel ureolytic soil archaeal ammonia oxidiser with tolerance to high ammonia concentration. FEMS Microbiol Ecol 2016;92:fiw057–10 [CrossRef]
    [Google Scholar]
  29. Jung MY, Kim JG, Sinninghe Damsté JS, Rijpstra WI, Madsen EL et al. A hydrophobic ammonia-oxidizing archaeon of the Nitrosocosmicus clade isolated from coal tar-contaminated sediment. Environ Microbiol Rep 2016;8:983–992 [CrossRef][PubMed]
    [Google Scholar]
  30. Spang A, Poehlein A, Offre P, Zumbrägel S, Haider S et al. The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 2012;14:3122–3145 [CrossRef][PubMed]
    [Google Scholar]
  31. Abby SS, Melcher M, Kerou M, Krupovic M, Stieglmeier M et al. Candidatus Nitrosocaldus cavascurensis, an ammonia oxidizing, extremely thermophilic archaeon with a highly mobile genome. Front Microbiol 2018;9:28 [CrossRef][PubMed]
    [Google Scholar]
  32. Daebeler A, Herbold CW, Vierheilig J, Sedlacek CJ, Pjevac P et al. Cultivation and genomic analysis of “Candidatus Nitrosocaldus islandicus,” an obligately thermophilic, ammonia-oxidizing Thaumarchaeon from a hot Spring biofilm in Graendalur Valley, Iceland. Front Microbiol 2018;9:193 [CrossRef][PubMed]
    [Google Scholar]
  33. de La Torre JR, Walker CB, Ingalls AE, Könneke M, Stahl DA. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 2008;10:810–818 [CrossRef][PubMed]
    [Google Scholar]
  34. Lebedeva EV, Hatzenpichler R, Pelletier E, Schuster N, Hauzmayer S 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 2013;8:e80835 [CrossRef][PubMed]
    [Google Scholar]
  35. Li Y, Ding K, Wen X, Zhang B, Shen B et al. A novel ammonia-oxidizing archaeon from wastewater treatment plant: Its enrichment, physiological and genomic characteristics. Sci Rep 2016;6:23747 [CrossRef][PubMed]
    [Google Scholar]
  36. Sauder LA, Albertsen M, Engel K, Schwarz J, Nielsen PH et al. Cultivation and characterization of Candidatus Nitrosocosmicus exaquare, an ammonia-oxidizing archaeon from a municipal wastewater treatment system. ISME J 2017;11:1142–1157 [CrossRef][PubMed]
    [Google Scholar]
  37. Sauder LA, Engel K, Lo C-C CP, Neufeld JD. Cultivation and characterization of Candidatus Nitrosotenuis aquariensis, an ammonia-oxidizing archaeon from a freshwater aquarium biofilter. Appl Environ Microbiol 2018;AEM.01430-18
    [Google Scholar]
  38. Qin W, Amin SA, Martens-Habbena W, Walker CB, Urakawa H et al. Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc Natl Acad Sci USA 2014;111:12504–12509 [CrossRef][PubMed]
    [Google Scholar]
  39. Carini P, Dupont CL, Santoro AE. Patterns of thaumarchaeal gene expression in culture and diverse marine environments. Environ Microbiol 2018;20:2112–2124 [CrossRef][PubMed]
    [Google Scholar]
  40. Palatinszky M, Herbold C, Jehmlich N, Pogoda M, Han P et al. Cyanate as an energy source for nitrifiers. Nature 2015;524:105–108 [CrossRef][PubMed]
    [Google Scholar]
  41. Kim JG, Park SJ, Sinninghe Damsté JS, Schouten S, Rijpstra WI et al. Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proc Natl Acad Sci USA 2016;113:7888–7893 [CrossRef][PubMed]
    [Google Scholar]
  42. Heal KR, Qin W, Ribalet F, Bertagnolli AD, Coyote-Maestas W et al. Two distinct pools of B12 analogs reveal community interdependencies in the ocean. Proc Natl Acad Sci USA 2017;114:364–369 [CrossRef][PubMed]
    [Google Scholar]
  43. Walker CB, de La Torre JR, Klotz MG, Urakawa H, Pinel N et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 2010;107:8818–8823 [CrossRef][PubMed]
    [Google Scholar]
  44. Stieglmeier M, Klingl A, Alves RJ, Rittmann SK, Melcher M et al. Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota. Int J Syst Evol Microbiol 2014;64:2738–2752 [CrossRef][PubMed]
    [Google Scholar]
  45. Holmes RM, Aminot A, Kérouel R, Hooker BA, Peterson BJ. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can J Fish Aquat Sci 1999;56:1801–1808 [CrossRef]
    [Google Scholar]
  46. Griess P. Bemerkungen zu der Abhandlung der HH. Weselsky und Benedikt "Über einige Azoverbindungen". Chem Ber 1879;12:426–428 [CrossRef]
    [Google Scholar]
  47. Marie D, Brussaard CPD, Thyrhaug R, Bratbak G, Vaulot D. Enumeration of marine viruses in culture and natural samples by flow cytometry. Appl Environ Microbiol 1999;65:45–52[PubMed]
    [Google Scholar]
  48. Herndl GJ, Reinthaler T, Teira E, van Aken H, Veth C et al. Contribution of archaea to total prokaryotic production in the deep Atlantic Ocean. Appl Environ Microbiol 2005;71:2303–2309 [CrossRef][PubMed]
    [Google Scholar]
  49. Tovar-Sanchez A, Sañudo-Wilhelmy SA, Garcia-Vargas M, Weaver RS, Popels LC et al. A trace metal clean reagent to remove surface-bound iron from marine phytoplankton. Mar Chem 2003;82:91–99 [CrossRef]
    [Google Scholar]
  50. Anderegg G, Arnaud-Neu F, Delgado R, Felcman J, Popov K. Critical evaluation of stability constants of metal complexes of complexones for biomedical and environmental applications* (IUPAC Technical Report). Pure and Applied Chemistry 2005;77:1445–1495 [CrossRef]
    [Google Scholar]
  51. Elling FJ, Könneke M, Nicol GW, Stieglmeier M, Bayer B et al. Chemotaxonomic characterisation of the thaumarchaeal lipidome. Environ Microbiol 2017;19:2681–2700 [CrossRef][PubMed]
    [Google Scholar]
  52. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013;30:772–780 [CrossRef][PubMed]
    [Google Scholar]
  53. Criscuolo A, Gribaldo S, Bmge GS. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol 2010;10:210 [CrossRef][PubMed]
    [Google Scholar]
  54. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015;32:268–274 [CrossRef][PubMed]
    [Google Scholar]
  55. Martens-Habbena W, Berube PM, Urakawa H, de La Torre JR, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 2009;461:976–979 [CrossRef][PubMed]
    [Google Scholar]
  56. Peng X, Fuchsman CA, Jayakumar A, Oleynik S, Martens-Habbena W et al. Ammonia and nitrite oxidation in the Eastern Tropical North Pacific. Global Biogeochem Cycles 2015;29:2034–2049 [CrossRef]
    [Google Scholar]
  57. Santoro AE, Casciotti KL, Francis CA. abundance and diversity of nitrifying archaea. Environ Microbiol 2010;12:1989–2006
    [Google Scholar]
  58. Varela MM, van Aken HM, Sintes E, Reinthaler T, Herndl GJ. Contribution of Crenarchaeota and Bacteria to autotrophy in the North Atlantic interior. Environ Microbiol 2011;13:1524–1533 [CrossRef][PubMed]
    [Google Scholar]
  59. Clark DR, Rees AP, Joint I. Ammonium regeneration and nitrification rates in the oligotrophic Atlantic Ocean: Implications for new production estimates. Limnol Oceanogr 2008;53:52–62 [CrossRef]
    [Google Scholar]
  60. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 2005;102:14683–14688 [CrossRef][PubMed]
    [Google Scholar]
  61. Glover HE. The relationship between inorganic nitrogen oxidation and organic carbon production in batch and chemostat cultures of marine nitrifying bacteria. Arch Microbiol 1985;142:45–50 [CrossRef]
    [Google Scholar]
  62. Könneke M, Schubert DM, Brown PC, Hügler M, Standfest S et al. Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation. Proc Natl Acad Sci USA 2014;111:8239–8244 [CrossRef][PubMed]
    [Google Scholar]
  63. Kozlowski JA, Stieglmeier M, Schleper C, Klotz MG, Stein LY. Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J 2016;10:1836–1845 [CrossRef][PubMed]
    [Google Scholar]
  64. Yan J, Haaijer SC, Op den Camp HJ, van Niftrik L, Stahl DA et al. Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ Microbiol 2012;14:3146–3158 [CrossRef][PubMed]
    [Google Scholar]
  65. Martens-Habbena W, Qin W, Horak RE, Urakawa H, Schauer AJ et al. The production of nitric oxide by marine ammonia-oxidizing archaea and inhibition of archaeal ammonia oxidation by a nitric oxide scavenger. Environ Microbiol 2015;17:2261–2274 [CrossRef][PubMed]
    [Google Scholar]
  66. Srithep P, Pornkulwat P, Limpiyakorn T. Contribution of ammonia-oxidizing archaea and ammonia-oxidizing bacteria to ammonia oxidation in two nitrifying reactors. Environ Sci Pollut Res Int 2018;25:8676–8687 [CrossRef][PubMed]
    [Google Scholar]
  67. Jung MY, Well R, Min D, Giesemann A, Park SJ et al. Isotopic signatures of N2O produced by ammonia-oxidizing archaea from soils. ISME J 2014;8:1115–1125 [CrossRef][PubMed]
    [Google Scholar]
  68. Offre P, Kerou M, Spang A, Schleper C. Variability of the transporter gene complement in ammonia-oxidizing archaea. Trends Microbiol 2014;22:665–675 [CrossRef][PubMed]
    [Google Scholar]
  69. Ouverney CC, Fuhrman JA. Marine planktonic archaea take up amino acids. Appl Environ Microbiol 2000;66:4829–4833 [CrossRef][PubMed]
    [Google Scholar]
  70. Björkman KM, Church MJ, Doggett JK, Karl DM. Differential assimilation of inorganic carbon and leucine by Prochlorococcus in the oligotrophic North Pacific subtropical gyre. Front Microbiol 2015;6:1401 [CrossRef][PubMed]
    [Google Scholar]
  71. Cunningham BR, John SG. The effect of iron limitation on cyanobacteria major nutrient and trace element stoichiometry. Limnol Oceanogr 2017;62:846–858 [CrossRef]
    [Google Scholar]
  72. Coleman JE. Zinc proteins: enzymes, storage proteins, transcription factors, and replication proteins. Annu Rev Biochem 1992;61:897–946 [CrossRef][PubMed]
    [Google Scholar]
  73. Amin SA, Moffett JW, Martens-Habbena W, Jacquot JE, Han Y et al. Copper requirements of the ammonia-oxidizing archaeon Nitrosopumilus maritimus SCM1 and implications for nitrification in the marine environment. Limnol Oceanogr 2013;58:2037–2045 [CrossRef]
    [Google Scholar]
  74. Smith JM, Chavez FP, Francis CA. Ammonium uptake by phytoplankton regulates nitrification in the sunlit ocean. PLoS One 2014;9:e108173 [CrossRef][PubMed]
    [Google Scholar]
  75. Horak REA, Qin W, Bertagnolli AD, Nelson A, Heal KR et al. Relative impacts of light, temperature, and reactive oxygen on thaumarchaeal ammonia oxidation in the North Pacific Ocean. Limnol Oceanogr 2018;63:741–757 [CrossRef]
    [Google Scholar]
  76. Tolar BB, Powers LC, Miller WL, Wallsgrove NJ, Popp BN et al. Ammonia oxidation in the ocean can be inhibited by nanomolar concentrations of hydrogen peroxide. Front Mar Sci 2016;3:237 [CrossRef]
    [Google Scholar]
  77. Jarrell KF, Ding Y, Nair DB, Siu S. Surface appendages of archaea: structure, function, genetics and assembly. Life 2013;3:86–117 [CrossRef][PubMed]
    [Google Scholar]
  78. Elling FJ, Becker KW, Könneke M, Schröder JM, Kellermann MY et al. Respiratory quinones in archaea: phylogenetic distribution and application as biomarkers in the marine environment. Environ Microbiol 2016;18:692–707 [CrossRef][PubMed]
    [Google Scholar]
  79. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 2008;6:245–252 [CrossRef][PubMed]
    [Google Scholar]
  80. Parks DH, Chuvochina M, Waite DW, Rinke C, Skarshewski A et al. A proposal for a standardized bacterial taxonomy based on genome phylogeny. Nat Biotechnol 2018;36:996–1004
    [Google Scholar]
  81. Blainey PC, Mosier AC, Potanina A, Francis CA, Quake SR. Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS One 2011;6:e16626 [CrossRef][PubMed]
    [Google Scholar]
  82. Jung MY, Islam MA, Gwak JH, Kim JG, Rhee SK. Nitrosarchaeum koreense gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon member of the phylum Thaumarchaeota isolated from agricultural soil. Int J Syst Evol Microbiol 2018;68:3084–3095 [CrossRef][PubMed]
    [Google Scholar]
  83. Lehtovirta-Morley LE, Sayavedra-Soto LA, Gallois N, Schouten S, Stein LY et al. Identifying potential mechanisms enabling acidophily in the ammonia-oxidizing archaeon “Candidatus Nitrosotalea devanaterra”. Appl Environ Microbiol 2016;82:2608–2619 [CrossRef]
    [Google Scholar]
  84. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci USA 2006;103:18296–18301 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.003360
Loading
/content/journal/ijsem/10.1099/ijsem.0.003360
Loading

Data & Media loading...

Supplementary data

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error