1887

Abstract

Two obligately acidophilic, mesophilic and aerobic soil ammonia-oxidising archaea were isolated from a pH 4.5 arable sandy loam (UK) and pH 4.7 acidic sulphate paddy soil (PR China) and designated strains Nd1 and Nd2, respectively. The strains shared more than 99 % 16S rRNA gene sequence identity and their genomes were both less than 2 Mb in length, sharing 79 % average nucleotide identity, 81 % average amino acid identity and a DNA G+C content of approximately 37 mol%. Both strains were chemolithotrophs that fixed carbon dioxide and gained energy by oxidising ammonia to nitrite, with no evidence of mixotrophic growth. Neither strain was capable of using urea as a source of ammonia. Both strains were non-motile in culture, although Nd1 does possess genes encoding flagella components and therefore may be motile under certain conditions. Cells of Nd1 were small angular rods 0.5–1 µm in length and grew at pH 4.2–5.6 and at 20–30 °C. Cells of Nd1 were small angular rods 0.5–1 µm in length and grew at pH 4.0–6.1 and at 20–42 °C. Nd1 and Nd2 are distinct with respect to genomic and physiological features and are assigned as the type strains for the species sp. nov. (type strain, Nd1=NCIMB 15248=DSM 110862) and sp. nov. (type strain, Nd2=NCIMB 15249=DSM 110863), respectively, within the genus gen. nov. The family fam. nov. and order ord. nov. are also proposed officially.

Funding
This study was supported by the:
  • Natural Environment Research Council (Award NE/I027835/1)
    • Principle Award Recipient: GraemeW Nicol
  • Natural Environment Research Council (Award NE/D010195/1)
    • Principle Award Recipient: GraemeW Nicol
  • Royal Society (Award DH150187)
    • Principle Award Recipient: LauraE. Lehtovirta-Morley
  • Royal Society (Award UF150571)
    • Principle Award Recipient: CécileGubry-Rangin
  • AXA Research Fund (Award AXA Chair in Microbial Ecology)
    • Principle Award Recipient: GraemeW Nicol
  • Royal Society (Award IE111001)
    • Principle Award Recipient: JamesI Prosser
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006387
2024-09-30
2024-10-05
Loading full text...

Full text loading...

References

  1. Frankland PF, Frankland G. The nitrifying process and its specific ferment.. Phil Trans R Soc B 1890; B181:107–128 [View Article]
    [Google Scholar]
  2. 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 [View Article] [PubMed]
    [Google Scholar]
  3. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004; 304:66–74 [View Article] [PubMed]
    [Google Scholar]
  4. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk H-P et al. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 2005; 7:1985–1995 [View Article] [PubMed]
    [Google Scholar]
  5. Oren A, Garrity GM. Valid publication of the names of forty-two phyla of prokaryotes. Int J Syst Evol Microbiol 2021; 71:005056 [View Article]
    [Google Scholar]
  6. 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 [View Article] [PubMed]
    [Google Scholar]
  7. Rinke C, Chuvochina M, Mussig AJ, Chaumeil P-A, Davín AA et al. A standardized archaeal taxonomy for the genome taxonomy database. Nat Microbiol 2021; 6:946–959 [View Article] [PubMed]
    [Google Scholar]
  8. Nicol GW, Leininger S, Schleper C. Distribution and activity of ammonia-oxidizing archaea in natural environments. In Ward BB, Klotz MG, Arp DJ. eds Nitrification Washington, DC: ASM Press; 2011 pp 157–178 [View Article]
    [Google Scholar]
  9. Ward BB. Nitrification in the ocean. In Ward BB, Klotz MG, Arp DJ. eds Nitrification Washington, DC: ASM Press; 2011 pp 325–345 [View Article]
    [Google Scholar]
  10. Prosser JI, Hink L, Gubry-Rangin C, Nicol GW. Nitrous oxide production by ammonia oxidizers: physiological diversity, niche differentiation and potential mitigation strategies. Glob Chang Biol 2020; 26:103–118 [View Article] [PubMed]
    [Google Scholar]
  11. 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 [View Article] [PubMed]
    [Google Scholar]
  12. Prosser JI, Nicol GW. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 2012; 20:523–531 [View Article] [PubMed]
    [Google Scholar]
  13. Jiang QQ, Bakken LR. Comparison of Nitrosospira strains isolated from terrestrial environments. FEMS Microbiol Ecol 1999; 30:171–186 [View Article] [PubMed]
    [Google Scholar]
  14. Urakawa H, Garcia JC, Nielsen JL, Le VQ, Kozlowski JA et al. Nitrosospira lacus sp. nov., a psychrotolerant, ammonia-oxidizing bacterium from sandy lake sediment. Int J Syst Evol Microbiol 2015; 65:242–250 [View Article]
    [Google Scholar]
  15. Hayatsu M, Tago K, Uchiyama I, Toyoda A, Wang Y et al. An acid-tolerant ammonia-oxidizing γ-proteobacterium from soil. ISME J 2017; 11:1130–1141 [View Article] [PubMed]
    [Google Scholar]
  16. Gubry-Rangin C, Nicol GW, Prosser JI. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 2010; 74:566–574 [View Article] [PubMed]
    [Google Scholar]
  17. Zhang L-M, Hu HW, Shen J-P, He J-Z. Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J 2012; 6:1032–1045 [View Article] [PubMed]
    [Google Scholar]
  18. Lehtovirta-Morley LE, Stöcker K, Vilcinskas A, Prosser JI, Nicol GW. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci U S A 2011; 108:15892–15897 [View Article] [PubMed]
    [Google Scholar]
  19. Kemp JS, Paterson E, Gammack SM, Cresser MS, Killham K. Leaching of genetically modified Pseudomonas fluorescens through organic soils: influence of temperature, soil pH, and roots. Biol Fertil Soils 1992; 13:218–224 [View Article]
    [Google Scholar]
  20. Paterson E, Kemp JS, Gammack SM, FitzPatrick EA, Cresser MS et al. Leaching of genetically modified Pseudomonas fluorescens through intact soil microcosms: influence of soil type. Biol Fertil Soils 1993; 15:308–314 [View Article]
    [Google Scholar]
  21. Lehtovirta-Morley LE, Ge C, Ross J, Yao H, Nicol GW et al. Characterisation of terrestrial acidophilic archaeal ammonia oxidisers and their inhibition and stimulation by organic compounds. FEMS Microbiol Ecol 2014; 89:542–552 [View Article] [PubMed]
    [Google Scholar]
  22. Allison SM, Prosser JI. Isolation and identification of autotrophic nitrifying bacteria. In Board RG, Jones D. eds Identification Methods in Applied and Environmental Microbiology Oxford: Blackwell Scientific Publications; 1992 pp 87–102
    [Google Scholar]
  23. Klein T, Poghosyan L, Barclay JE, Murrell JC, Hutchings MI et al. Cultivation of ammonia-oxidising archaea on solid medium. FEMS Microbiol Lett 2022; 369:fnac029 [View Article] [PubMed]
    [Google Scholar]
  24. Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC et al. Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci U S A 2011; 108:21206–21211 [View Article] [PubMed]
    [Google Scholar]
  25. Alves RJE, Minh BQ, Urich T, von Haeseler A, Schleper C. Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat Commun 2018; 9:1517 [View Article] [PubMed]
    [Google Scholar]
  26. Jung M-Y, Park S-J, Kim S-J, Kim J-G, 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 [View Article] [PubMed]
    [Google Scholar]
  27. Herbold CW, Lehtovirta-Morley LE, Jung M-Y, Jehmlich N, Hausmann B et al. Ammonia-oxidising archaea living at low pH: insights from comparative genomics. Environ Microbiol 2017; 19:4939–4952 [View Article] [PubMed]
    [Google Scholar]
  28. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
    [Google Scholar]
  29. Prosser JI, Nicol GW. Family: Candidatus Nitrosotaleaceae fam. nov. In Whitman WB. eds Bergey’s Manual of Systematic Bacteriology Oxford: John Wiley and Sons; 2016 [View Article]
    [Google Scholar]
  30. Stieglmeier M, Klingl A, Alves RJE, Rittmann SK-MR, 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 [View Article] [PubMed]
    [Google Scholar]
  31. 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 [View Article] [PubMed]
    [Google Scholar]
  32. 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 [View Article] [PubMed]
    [Google Scholar]
  33. Tourna M, Stieglmeier M, Spang A, Könneke M, Schintlmeister A et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 2011; 108:8420–8425 [View Article] [PubMed]
    [Google Scholar]
  34. 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 [View Article] [PubMed]
    [Google Scholar]
  35. Qin W, Jewell TNM, de la Torre BP et al. Candidatus Nitrosocaldales. In Whitman WB. eds Bergey’s Manual of Systematic Bacteriology Oxford: John Wiley and Sons; 2017 [View Article]
    [Google Scholar]
  36. 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 [View Article] [PubMed]
    [Google Scholar]
  37. Elling FJ, Könneke M, Nicol GW, Stieglmeier M, Bayer B et al. Chemotaxonomic characterisation of the thaumarchaeal lipidome. Environ Microbiol 2017; 19:2681–2700 [View Article] [PubMed]
    [Google Scholar]
  38. Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM et al. Biological nitrification inhibition (BNI)—is it a widespread phenomenon?. Plant Soil 2007; 294:5–18 [View Article]
    [Google Scholar]
  39. Lehtovirta-Morley LE, Verhamme DT, Nicol GW, Prosser JI. Effect of nitrification inhibitors on the growth and activity of Nitrosotalea devanaterra in culture and soil. Soil Biol Biochem 2013; 62:129–133 [View Article]
    [Google Scholar]
  40. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A et al. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci U S A 2008; 105:2134–2139 [View Article] [PubMed]
    [Google Scholar]
  41. Taylor AE, Zeglin LH, Dooley S, Myrold DD, Bottomley PJ. Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse Oregon soils. Appl Environ Microbiol 2010; 76:7691–7698 [View Article] [PubMed]
    [Google Scholar]
  42. Jung M-Y, Park S-J, Min D, Kim J-S, Rijpstra WIC et al. Enrichment and characterization of an autotrophic ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. Appl Environ Microbiol 2011; 77:8635–8647 [View Article] [PubMed]
    [Google Scholar]
  43. Kim J-G, Park S-J, Sinninghe Damsté JS, Schouten S, Rijpstra WIC et al. Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proc Natl Acad Sci U S A 2016; 113:7888–7893 [View Article] [PubMed]
    [Google Scholar]
  44. Aigle A, Prosser JI, Gubry-Rangin C. The application of high-throughput sequencing technology to analysis of amoA phylogeny and environmental niche specialisation of terrestrial bacterial ammonia-oxidisers. Environ Microbiome 2019; 14:3 [View Article] [PubMed]
    [Google Scholar]
  45. De Boer W, Gunnewiek PJ, Veenhuis M, Bock E, Laanbroek HJ. Nitrification at low pH by aggregated chemolithotrophic bacteria. Appl Environ Microbiol 1991; 57:3600–3604 [View Article] [PubMed]
    [Google Scholar]
  46. Wang Z, Zheng M, Meng J, Hu Z, Ni G et al. Robust nitritation sustained by acid-tolerant ammonia-oxidizing bacteria. Environ Sci Technol 2021; 55:2048–2056 [View Article]
    [Google Scholar]
  47. Picone N, Pol A, Mesman R, van Kessel MAHJ, Cremers G et al. Ammonia oxidation at pH 2.5 by a new gammaproteobacterial ammonia-oxidizing bacterium. ISME J 2021; 15:1150–1164 [View Article] [PubMed]
    [Google Scholar]
  48. Jung M-Y, Sedlacek CJ, Kits KD, Mueller AJ, Rhee S-K et al. Ammonia-oxidizing archaea possess a wide range of cellular ammonia affinities. ISME J 2022; 16:272–283 [View Article] [PubMed]
    [Google Scholar]
  49. Hink L, Gubry-Rangin C, Nicol GW, Prosser JI. The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J 2018; 12:1084–1093 [View Article] [PubMed]
    [Google Scholar]
  50. Qin W, Jewell TNM, Russell VV, de la Torre BP et al. Candidatus Nitrosocaldales. In Whitman WB. eds Bergey’s Manual Systematic Bacteriol Oxford: John Wiley and Sons; 2017 [View Article]
    [Google Scholar]
  51. 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 [View Article] [PubMed]
    [Google Scholar]
  52. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article] [PubMed]
    [Google Scholar]
  53. Lee MD. GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 2019; 35:4162–4164 [View Article] [PubMed]
    [Google Scholar]
  54. Bayer B, Vojvoda J, Reinthaler T, Reyes C, Pinto M et al. Nitrosopumilus adriaticus sp. nov. and Nitrosopumilus piranensis sp. nov., two ammonia-oxidizing archaea from the Adriatic Sea and members of the class Nitrososphaeria. Int J Syst Evol Microbiol 2019; 69:1892–1902 [View Article] [PubMed]
    [Google Scholar]
  55. Nakagawa T, Koji M, Hosoyama A, Yamazoe A, Tsuchiya Y et al. Nitrosopumilus zosterae sp. nov., an autotrophic ammonia-oxidizing archaeon of phylum Thaumarchaeota isolated from coastal eelgrass sediments of Japan. Int J Syst Evol Microbiol 2021; 71:004961 [View Article] [PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.006387
Loading
/content/journal/ijsem/10.1099/ijsem.0.006387
Loading

Data & Media loading...

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