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PMID: 20870784 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Cultivation of autotrophic ammonia-oxidizing archaea from marine sediments in coculture with sulfur-oxidizing bacteria.

Applied and environmental microbiology ·Vol. 76 ·No. 22 ·2010-11-00 ·Pages 7575-87

Park BJ, Park SJ, Yoon DN, Schouten S, Sinninghe Damsté JS, Rhee SK

Abstract

The role of ammonia-oxidizing archaea (AOA) in nitrogen cycling in marine sediments remains poorly characterized. In this study, we enriched and characterized AOA from marine sediments. Group I.1a crenarchaea closely related to those identified in marine sediments and "Candidatus Nitrosopumilus maritimus" (99.1 and 94.9% 16S rRNA and amoA gene sequence identities to the latter, respectively) were substantially enriched by coculture with sulfur-oxidizing bacteria (SOB). The selective enrichment of AOA over ammonia-oxidizing bacteria (AOB) is likely due to the reduced oxygen levels caused by the rapid initial growth of SOB. After biweekly transfers for ca. 20 months, archaeal cells became the dominant prokaryotes (>80%), based on quantitative PCR and fluorescence in situ hybridization analysis. The increase of archaeal 16S rRNA gene copy numbers was coincident with the amount of ammonia oxidized, and expression of the archaeal amoA gene was observed during ammonia oxidation. Bacterial amoA genes were not detected in the enrichment culture. The affinities of these AOA to oxygen and ammonia were substantially higher than those of AOB. [(13)C]bicarbonate incorporation and the presence and activation of genes of the 3-hydroxypropionate/4-hydroxybutyrate cycle indicated autotrophy during ammonia oxidation. In the enrichment culture, ammonium was oxidized to nitrite by the AOA and subsequently to nitrate by Nitrospina-like bacteria. Our experiments suggest that AOA may be important nitrifiers in low-oxygen environments, such as oxygen-minimum zones and marine sediments.

MeSH Terms
Ammonia/metabolism Archaea/classification,growth & development,isolation & purification,metabolism Bacteria/classification,growth & development,isolation & purification,metabolism Cluster Analysis Coculture Techniques DNA, Archaeal/chemistry,genetics DNA, Bacterial/chemistry,genetics DNA, Ribosomal/chemistry,genetics DNA, Ribosomal Spacer/chemistry,genetics Genes, rRNA Geologic Sediments/microbiology Molecular Sequence Data Oxidation-Reduction Phylogeny RNA, Archaeal/genetics RNA, Bacterial/genetics RNA, Ribosomal, 16S/genetics Sequence Analysis, DNA Sequence Homology, Nucleic Acid Sulfur/metabolism
Chemicals
DNA, Archaeal DNA, Bacterial DNA, Ribosomal DNA, Ribosomal Spacer RNA, Archaeal RNA, Bacterial RNA, Ribosomal, 16S Sulfur Ammonia
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Park Byoung-Joon
Department of Microbiology, Chungbuk National University, Heungduk-gu, Cheongju 361-763, South Korea.
Park Soo-Je
Yoon Dae-No
Schouten Stefan
Sinninghe Damsté Jaap S
Rhee Sung-Keun
References (75)
75 references, click to expand
  1. Ammonia-oxidizing archaea: important players in paddy rhizosphere soil?
    Environ Microbiol. 2008 Aug;10(8):1978-87 PMID: 18430011
  2. Autotrophic nitrification in bacteria.
    Adv Microb Physiol. 1989;30:125-81 PMID: 2700538
  3. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea.
    Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7104-9 PMID: 17420469
  4. Marine planktonic archaea take up amino acids.
    Appl Environ Microbiol. 2000 Nov;66(11):4829-33 PMID: 11055931
  5. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean.
    Proc Natl Acad Sci U S A. 2005 Oct 11;102(41):14683-8 PMID: 16186488
  6. 13C-isotope analyses reveal that chemolithoautotrophic Gamma- and Epsilonproteobacteria feed a microbial food web in a pelagic redoxcline of the central Baltic Sea.
    Environ Microbiol. 2009 Feb;11(2):326-37 PMID: 18793316
  7. Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota.
    Trends Microbiol. 2010 Aug;18(8):331-40 PMID: 20598889
  8. Improvements in epoxy resin embedding methods.
    J Biophys Biochem Cytol. 1961 Feb;9:409-14 PMID: 13764136
  9. Environmental genome shotgun sequencing of the Sargasso Sea.
    Science. 2004 Apr 2;304(5667):66-74 PMID: 15001713
  10. Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment.
    Proc Natl Acad Sci U S A. 2008 Jul 29;105(30):10583-8 PMID: 18650394
  11. Impact of prehybridization PCR amplification on microarray detection of nitrifying bacteria in wastewater treatment plant samples.
    Environ Microbiol. 2006 Sep;8(9):1564-74 PMID: 16913917
  12. Significant contribution of Archaea to extant biomass in marine subsurface sediments.
    Nature. 2008 Aug 21;454(7207):991-4 PMID: 18641632
  13. Novel major archaebacterial group from marine plankton.
    Nature. 1992 Mar 12;356(6365):148-9 PMID: 1545865
  14. Improved colorimetric determination of urinary thiosulfate to study intermediate sulfur metabolism in humans.
    Clin Chem. 1993 Dec;39(12):2533-4 PMID: 8252731
  15. Archaea predominate among ammonia-oxidizing prokaryotes in soils.
    Nature. 2006 Aug 17;442(7104):806-9 PMID: 16915287
  16. Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria.
    Appl Environ Microbiol. 1996 Jun;62(6):2156-62 PMID: 8787412
  17. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling.
    Environ Microbiol. 2005 Dec;7(12):1985-95 PMID: 16309395
  18. Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria.
    J Bacteriol. 1994 Nov;176(21):6623-30 PMID: 7961414
  19. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol.
    Environ Microbiol. 2008 Mar;10(3):810-8 PMID: 18205821
  20. Diversity of thiosulfate-oxidizing bacteria from marine sediments and hydrothermal vents.
    Appl Environ Microbiol. 2000 Aug;66(8):3125-33 PMID: 10919760
  21. Archaea in coastal marine environments.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5685-9 PMID: 1608980
  22. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations.
    Appl Environ Microbiol. 1990 Jun;56(6):1919-25 PMID: 2200342
  23. Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota.
    J Lipid Res. 2002 Oct;43(10):1641-51 PMID: 12364548
  24. 16S ribosomal DNA amplification for phylogenetic study.
    J Bacteriol. 1991 Jan;173(2):697-703 PMID: 1987160
  25. Ammonia-oxidizing communities in a highly aerated full-scale activated sludge bioreactor: betaproteobacterial dynamics and low relative abundance of Crenarchaea.
    Environ Microbiol. 2009 Sep;11(9):2310-28 PMID: 19515200
  26. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea.
    Proc Natl Acad Sci U S A. 2010 May 11;107(19):8818-23 PMID: 20421470
  27. Comparative analysis of archaeal 16S rRNA and amoA genes to estimate the abundance and diversity of ammonia-oxidizing archaea in marine sediments.
    Extremophiles. 2008 Jul;12(4):605-15 PMID: 18465082
  28. A cold-loving crenarchaeon is a substantial part of a novel microbial community in cold sulphidic marsh water.
    FEMS Microbiol Ecol. 2006 Jul;57(1):55-66 PMID: 16819950
  29. Microeukaryotic diversity in marine environments, an analysis of surface layer sediments from the East Sea.
    J Microbiol. 2008 Jun;46(3):244-9 PMID: 18604492
  30. Bicarbonate uptake by marine Crenarchaeota.
    FEMS Microbiol Lett. 2003 Feb 28;219(2):203-7 PMID: 12620621
  31. Molecular and biogeochemical evidence for ammonia oxidation by marine Crenarchaeota in the Gulf of California.
    ISME J. 2008 Apr;2(4):429-41 PMID: 18200070
  32. Anaerobic ammonia-oxidizing bacteria and related activity in Baltimore inner harbor sediment.
    Appl Environ Microbiol. 2005 Apr;71(4):1816-21 PMID: 15812006
  33. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment.
    Brief Bioinform. 2004 Jun;5(2):150-63 PMID: 15260895
  34. Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments.
    Int J Syst Evol Microbiol. 2004 Sep;54(Pt 5):1477-1482 PMID: 15388698
  35. Pacific Northwest marine sediments contain ammonia-oxidizing bacteria in the beta subdivision of the Proteobacteria.
    Appl Environ Microbiol. 2000 Oct;66(10):4532-5 PMID: 11010911
  36. Anaerobic ammonium oxidation (anammox) in the marine environment.
    Res Microbiol. 2005 May;156(4):457-64 PMID: 15862442
  37. Alcanivorax dieselolei sp. nov., a novel alkane-degrading bacterium isolated from sea water and deep-sea sediment.
    Int J Syst Evol Microbiol. 2005 May;55(Pt 3):1181-1186 PMID: 15879252
  38. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea.
    FEMS Microbiol Rev. 2009 Sep;33(5):855-69 PMID: 19453522
  39. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota.
    Nat Rev Microbiol. 2008 Mar;6(3):245-52 PMID: 18274537
  40. Diversity and spatial distribution of sediment ammonia-oxidizing crenarchaeota in response to estuarine and environmental gradients in the Changjiang Estuary and East China Sea.
    Microbiology (Reading). 2008 Jul;154(Pt 7):2084-2095 PMID: 18599836
  41. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota.
    PLoS Biol. 2006 Apr;4(4):e95 PMID: 16533068
  42. Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre.
    Environ Microbiol. 2007 May;9(5):1162-75 PMID: 17472632
  43. Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of Group I.
    Mol Ecol. 2000 Jul;9(7):935-48 PMID: 10886656
  44. Archaeal ammonia oxidizers and nirS-type denitrifiers dominate sediment nitrifying and denitrifying populations in a subtropical macrotidal estuary.
    ISME J. 2010 Feb;4(2):286-300 PMID: 19798039
  45. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring.
    Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):2134-9 PMID: 18250313
  46. Major gradients in putatively nitrifying and non-nitrifying Archaea in the deep North Atlantic.
    Nature. 2008 Dec 11;456(7223):788-91 PMID: 19037244
  47. Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon.
    Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6442-7 PMID: 16614070
  48. Isolation of an autotrophic ammonia-oxidizing marine archaeon.
    Nature. 2005 Sep 22;437(7058):543-6 PMID: 16177789
  49. Diversity of ammonia-oxidizing archaea and bacteria in the sediments of a hypernutrified subtropical estuary: Bahía del Tóbari, Mexico.
    Appl Environ Microbiol. 2006 Dec;72(12):7767-77 PMID: 17012598
  50. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria.
    Nature. 2009 Oct 15;461(7266):976-9 PMID: 19794413
  51. Putative ammonia-oxidizing Crenarchaeota in suboxic waters of the Black Sea: a basin-wide ecological study using 16S ribosomal and functional genes and membrane lipids.
    Environ Microbiol. 2007 Apr;9(4):1001-16 PMID: 17359272
  52. Archaeal dominance in the mesopelagic zone of the Pacific Ocean.
    Nature. 2001 Jan 25;409(6819):507-10 PMID: 11206545
  53. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations.
    Appl Environ Microbiol. 1997 Dec;63(12):4704-12 PMID: 9406389
  54. Contribution of Archaea to total prokaryotic production in the deep Atlantic Ocean.
    Appl Environ Microbiol. 2005 May;71(5):2303-9 PMID: 15870315
  55. Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea.
    ISME J. 2007 Dec;1(8):743-55 PMID: 18059497
  56. A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya.
    Biol Direct. 2008 Dec 23;3:54 PMID: 19105819
  57. Distribution of membrane lipids of planktonic Crenarchaeota in the Arabian Sea.
    Appl Environ Microbiol. 2002 Jun;68(6):2997-3002 PMID: 12039760
  58. Archaeal nitrification in the ocean.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12317-22 PMID: 16894176
  59. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA.
    Appl Environ Microbiol. 1993 Mar;59(3):695-700 PMID: 7683183
  60. Genomic studies of uncultivated archaea.
    Nat Rev Microbiol. 2005 Jun;3(6):479-88 PMID: 15931166
  61. The oligonucleotide probe database.
    Appl Environ Microbiol. 1996 Oct;62(10):3557-9 PMID: 8837410
  62. Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at station ALOHA in the North Pacific subtropical gyre.
    Appl Environ Microbiol. 2009 Aug;75(16):5345-55 PMID: 19542347
  63. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys.
    Appl Environ Microbiol. 2000 Dec;66(12):5368-82 PMID: 11097916
  64. Hoeflea alexandrii sp. nov., isolated from the toxic dinoflagellate Alexandrium minutum AL1V.
    Int J Syst Evol Microbiol. 2006 Aug;56(Pt 8):1991-1995 PMID: 16902042
  65. Dynamics of nitrification and denitrification in root-oxygenated sediments and adaptation of ammonia-oxidizing bacteria to low-oxygen or anoxic habitats.
    Appl Environ Microbiol. 1996 Nov;62(11):4100-7 PMID: 16535441
  66. Characterization of two ammonia-oxidizing bacteria isolated from reactors operated with low dissolved oxygen concentrations.
    J Appl Microbiol. 2007 May;102(5):1401-17 PMID: 17448175
  67. Kordiimonas gwangyangensis gen. nov., sp. nov., a marine bacterium isolated from marine sediments that forms a distinct phyletic lineage (Kordiimonadales ord. nov.) in the 'Alphaproteobacteria'.
    Int J Syst Evol Microbiol. 2005 Sep;55(Pt 5):2033-2037 PMID: 16166706
  68. Review and re-analysis of domain-specific 16S primers.
    J Microbiol Methods. 2003 Dec;55(3):541-55 PMID: 14607398
  69. Specific inhibition of nitrite oxidation by chlorate and its use in assessing nitrification in soils and sediments.
    Appl Environ Microbiol. 1980 Mar;39(3):505-10 PMID: 16345525
  70. Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru.
    Proc Natl Acad Sci U S A. 2006 Mar 7;103(10):3846-51 PMID: 16505362
  71. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea.
    Science. 2007 Dec 14;318(5857):1782-6 PMID: 18079405
  72. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  73. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.
    J Cell Biol. 1963 Apr;17:208-12 PMID: 13986422
  74. Phylogenetic identification and in situ detection of individual microbial cells without cultivation.
    Microbiol Rev. 1995 Mar;59(1):143-69 PMID: 7535888
  75. Prokaryotes: the unseen majority.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6578-83 PMID: 9618454
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
1098-5336
Published
2010-11-00
Epub
2010-00-24
Pages
7575-87
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC2976178
Subset
IM
Databases
GENBANK
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