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Archaeal nucleic acids in picoplankton from great lakes on three continents

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Abstract

Phylogenetic analysis of PCR-amplified 16S rRNA genes revealed the presence of archaea in picoplankton collected from the Laurentian Great Lakes in North America, Africa’s Lake Victoria, and Lakes Ladoga and Onega in northeastern Eurasia. From 1 to 10% of the rRNA extracted from size-fractionated picoplankton (>0.2 µm but <1.2 µm) collected in the epilimnion and hypolimnion of these lakes was specific to the Archaea, whereas the majority of rRNA was derived from Bacteria. Analysis of the 16S rRNA genes cloned from these samples indicated they were closely related to crenarchaeal sequences that have been widely characterized from marine environments. The presence of nearly identical 16S rDNA clones in several of these geographically disparate lakes suggests a cosmopolitan distribution of specific subgroups of these Archaea in freshwater environments. Despite their abundance in the water column of freshwater lakes, we have no representatives of these crenarchaea in pure culture, and so their physiological characteristics and ecological role remain unknown.

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References

  1. Aim EW, Oerther DB, Larsen N, Stahl DA, Raskin L (1996) The oligonucleotide probe database. Appl Environ Microbiol 62:3557–3559

    Google Scholar 

  2. Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental-studies in microbiology. J Bacteriol 172:762–770

    PubMed  CAS  Google Scholar 

  3. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in-situ detection of individual microbial-cells without cultivation. Microbiol Rev 59:143–169

    PubMed  CAS  Google Scholar 

  4. Bintrim SB, Donohue TJ, Handelsman J, Roberts GP, Goodman RM (1997) Molecular phylogeny of Archaea from soil. Proc Natl Acad Sci USA 94:277–282

    Article  PubMed  CAS  Google Scholar 

  5. Buckley DH, Graber JR, Schmidt TM (1998) Phylogenetic analysis of nonthermophilic members of the kingdom Crenarchaeota and their diversity and abundance in soils. Appl Environ Microbiol 64:4333–4339

    PubMed  CAS  Google Scholar 

  6. Burggraf S, Mayer T, Amann R, Schadhauser S, Woese CR, Stetter KO (1994) Identifying members of the Domain Archaea with ribosomal-RNA targeted oligonucleotide probes. Appl Environ Microbiol 60:3112–3119

    PubMed  CAS  Google Scholar 

  7. DeLong EF (1992) Archaea in coastal marine environments. Proc Natl Acad Sci USA 89:5685–5689

    Article  PubMed  CAS  Google Scholar 

  8. DeLong EF (1998) Everything in moderation: Archaea as “non-extremophiles”. Curr Opin Genet Dev 8:649–654

    Article  PubMed  CAS  Google Scholar 

  9. DeLong EF, King LL, Massana R, Cittone H, Murray A, Schleper C, Wakeham SG (1998) Dibiphytanyl ether lipids in nonthermophilic crenarchaeotes. Appl Environ Microbiol 64:1133–1138

    PubMed  CAS  Google Scholar 

  10. DeLong EF, Wu KY, Prezelin BB, Jovine RVM (1994) High abundance of Archaea in antarctic marine picoplankton. Nature 371:695–697

    Article  PubMed  CAS  Google Scholar 

  11. Engstrom DR, Fritz SC, Almendinger JE, Juggins S (2000) Chemical and biological trends during lake evolution in recently deglaciated terrain. Nature 408:161–166

    Article  PubMed  CAS  Google Scholar 

  12. Fuhrman JA, Campbell L (1998) Marine ecology—microbial microdiversity. Nature 393:410–411

    Article  CAS  Google Scholar 

  13. Fuhrman JA, Comeau DE, Hagstorm A, Chan AM (1998) Extraction from natural planktonic microorganisms of DNA suitable for molecular biological studies. Appl Environ Microbiol 54:1426–1429

    Google Scholar 

  14. Fuhrman JA, McCallum K, Davis AA (1992) Novel major archaebacterial group from marine plankton. Nature 356:148–149

    Article  PubMed  CAS  Google Scholar 

  15. Fuhrman JA, McCallum K, Davis AA (1993) Phylogenetic diversity of subsurface marine microbial communities from the Atlantic and Pacific Oceans. Appl Environ Microbiol 59:1294–1302

    PubMed  CAS  Google Scholar 

  16. Giovannoni SJ, Delong EF, Olsen GJ, Pace NR (1988) Phylogenetic group-specific oligodeoxynucleotide probes for identification of single microbial-cells. J Bacteriol 170:720–726

    PubMed  CAS  Google Scholar 

  17. Glockner FO, Fuchs BM, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65:3721–3726

    PubMed  CAS  Google Scholar 

  18. Hershberger KL, Barns SM, Reysenbach AL, Dawson SC, Pace NR (1996) Wide diversity of crenarchaeota. Nature 384:420–420

    Article  PubMed  CAS  Google Scholar 

  19. Hershey AE, Gettel GM, McDonald ME, Miller MC, Mooers H, O’Brien WJ, Pastor J, Richards C, Schuldt JA (1999) A geomorphic-trophic model for landscape control of lake food webs. Bioscience 49:887–897

    Article  Google Scholar 

  20. Hicks RE, Pascoe DA (2001) A comparison of cyanobacterial dominance within the picoplankton of the North American Great Lakes estimated by 16S rRNA-based hybridizations and direct cell counts. In: Munawar M, Hecky RE (Eds.) The Great Lakes of the World (GLOW): Food-Web, Health, and Integrity. Backhuys Publishers, Leiden, The Netherlands, pp 363–374

    Google Scholar 

  21. Jurgens G, Glockner FO, Amann R, Saano A, Montonen L, Likolammi M, Munster U (2000) Identification of novel Archaea in bacterioplankton of a boreal forest lake by phlogenetic analysis and fluorescent in situ hybridization. FEMS Microbiol Ecol 34:45–56

    PubMed  CAS  Google Scholar 

  22. Jurgens G, Lindstorm K, Saano A (1997) Novel group within the kingdom Crenarchaeota from boreal forest soil. Appl Environ Microbiol 63:803–805

    PubMed  CAS  Google Scholar 

  23. Kapustina LL (1996) Bacterioplankton response to eutrophication in Lake Ladoga. Hydrobiologia 322:17–22

    Article  Google Scholar 

  24. Karner MB, Delong EF, Karl DM (2001) Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409:507–510

    Article  PubMed  CAS  Google Scholar 

  25. Lathe R (1985) Synthetic oligonucleotide probes deduced from amino-acid sequence data-theoretical and practical considerations. J Mol Biol 183:1–12

    Article  PubMed  CAS  Google Scholar 

  26. Lee N, Nielsen PH, Andreasen KH, Jurestschko S, Nielsen JL, Schleifen KH, Wagner M (1999) Combination of fluorescent in situ hybridization and microautoradiography—a new tool for structure-function analyses in microbial ecology. Appl Environ Microbiol 65:1289–1297

    PubMed  CAS  Google Scholar 

  27. MacGregor BJ, Moser DP, Baker BJ, Aim EW, Maurer M, Nealson KH, Stahl DA (2001) Seasonal and spatial variability in Lake Michigan sediment small-subunit rRNA concentrations. Appl Environ Microbiol 67:3908–3922

    Article  PubMed  CAS  Google Scholar 

  28. MacGregor BJ, Moser DP, Aim EW, Nealson KH, Stahl DA (1997) Crenarchaeota in Lake Michigan sediment. Appl Environ Microbiol 63:1178–1181

    PubMed  CAS  Google Scholar 

  29. Massana R, DeLong EF, Pedros-Alio C (2000) A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Appl Environ Microbiol 66:1777–1787

    Article  PubMed  CAS  Google Scholar 

  30. Massana R, Murray AE, Preston CM, Delong EF (1997) Vertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel. Appl Environ Microbiol 63:50–56

    PubMed  CAS  Google Scholar 

  31. Murray AE, Preston CM, Massana R, Taylor LT, Blakis A, Wu K, Delong EF (1998) Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64:2585–2595

    PubMed  CAS  Google Scholar 

  32. Nold SC, Zwart G (1998) Patterns and governing forces in aquatic microbial communities. Aquat Ecol 32:17–35

    Article  CAS  Google Scholar 

  33. Olsen GJ, Matsuda H, Hagstrom R, Overbeek R (1994) FastDNAml—a tool for construction of phylogenetic trees of DNA-sequences using maximum-likelihood. Comput Appl Biosci 10:41–48

    PubMed  CAS  Google Scholar 

  34. Oren A, Lau PP, Fox GE (1988) The taxonomic status of Halobacterium marismortui from the Dead Sea-a comparison with Halobacterium vallismortis. Syst Appl Microbiol 10:251–258

    PubMed  CAS  Google Scholar 

  35. Ouverney CC, Fuhrman JA (1999) Combined microautoradiography-16S rRNA probe technique for determination of radioisotope uptake by specific microbial cell types in situ. Appl Environ Microbiol 65:1746–1752

    PubMed  CAS  Google Scholar 

  36. Pernthaler J, Glockner FO, Unterholzer S, Alfreider A, Psenner R, Amann R (1998) Seasonal community and population dynamics of pelagic bacteria and archaea in a high mountain lake. Appl Environ Microbiol 64:4299–4306

    PubMed  CAS  Google Scholar 

  37. Raskin L, Stromley JM, Rittmann BE, Stahl DA (1994) Group specific 16S ribosomal-RNA hybridization probes to describe natural communities of methanogens. Appl Environ Microbiol 60:1232–1240

    PubMed  CAS  Google Scholar 

  38. Riera JL, Magnuson JJ, Kratz TK, Webster KE (2000) A geomorphic template for the analysis of lake districts applied to the Northern Highland Lake District, Wisconsin, U.S.A. Freshwat Biol 43:301–318

    Article  Google Scholar 

  39. Saitou N, Neil M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  40. Sandaa RA, Enger O, Torsvik V (1999) Abundance and diversity of Archaea in heavy-metal-contaminated soils. Appl Environ Microbiol 65:3293–3297

    PubMed  CAS  Google Scholar 

  41. Schleper C, Holben W, Klenk HP (1997) Recovery of crenarchaeotal ribosomal DNA sequences from freshwater lake sediments. Appl Environ Microbiol 63:321–323

    PubMed  CAS  Google Scholar 

  42. Stahl DA, Amann R (1991) Development and application of nucleic acid probes in bacterial systematics. In: Stackebrandt E, Goodfellow M (Eds.) Nucleic Acid Techniques in Bacterial Systematics. John Wiley & Sons, Chichester, UK, pp 205–248

    Google Scholar 

  43. Stein LY, LaDuo MT, Grundl TJ, Nealson KH (2001) Bacterial and archaeal populations associated with freshwater ferromanganous micronodules and sediments. Environ Microbiol 3:10–18

    Article  PubMed  CAS  Google Scholar 

  44. Takai K, Moser DP, DeFlaun M, Onstott TC, Fredrickson JK (2001) Archaeal diversity waters from deep South African gold mines. Appl Environ Microbiol 67:5750–5760

    Article  PubMed  CAS  Google Scholar 

  45. Tsai YL, Olson BH (1992) Rapid method for separation of bacterial-DNA from humic substances in sediments for polymerase chain-reaction. Appl Environ Microbiol 58: 2292–2295

    PubMed  CAS  Google Scholar 

  46. Van Mooy B, MacGregor B, Hollander D, Nealson K, Stahl D (2001) Evidence of tight coupling between active bacteria and particulate organic carbon during seasonal stratification of Lake Michigan. Limnol Oceanogr 46:1202–1208

    Article  Google Scholar 

  47. Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW (2002) Extensive fungal diversity in plant roots. Science 295:2051

    Article  PubMed  Google Scholar 

  48. Verschuren D, Edgington DN, Kling HJ, Johnson TC (1998) Silica depletion in Lake Victoria: Sedimentary signals at offshore stations. J Gt Lakes Res 24:118–130

    CAS  Google Scholar 

  49. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms—proposal for the domain Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

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Author notes

  1. B. P. Keough

    Present address: Department of Microbiology and Molecular Genetics, Michigan State University, Bio-Physical Sciences Building, 48823, East Lansing, MI

Authors and Affiliations

  1. University of Minnesota - Duluth, Duluth, MN, USA

    B. P. Keough & R. E. Hicks

  2. Michigan State University, East Lansing, MI, USA

    T. M. Schmidt

Authors
  1. B. P. Keough
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  2. T. M. Schmidt
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  3. R. E. Hicks
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Corresponding author

Correspondence to B. P. Keough.

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Online publication: 6 June 2003

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Keough, B.P., Schmidt, T.M. & Hicks, R.E. Archaeal nucleic acids in picoplankton from great lakes on three continents. Microb Ecol 46, 238–248 (2003). https://doi.org/10.1007/s00248-003-1003-1

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