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Biogeography and Landscape-Scale Diversity of the Dominant Crenarchaeota of Soil

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Abstract

We surveyed the diversity of soil Archaea across a large scale elevational gradient of ecosystem types, from foothills forest to alpine tundra in the Front Range of the Rocky Mountains. We used a dilution technique to sequence the single most abundant archaeal 16S rDNA sequence in each of the 40 soil cores distributed across the gradient to compare our results to those of typical 16S clone library studies.We found a greater diversity of sequences than has typically been found in clone library studies from a single site or core, identifying sequences both from the Terrestrial Group and the FFSB Group at several sites. We did not observe any significant environmental correlates with the dominant sequence type, nor was there any relationship between the spatial distance between samples and the phylogenetic similarity of the dominant sequence types. Despite using a very different methodology, our collective results are in remarkably good agreement with other studies of soil Crenarchaeota in terms of the diversity and relative abundance of sequence types identified. We are able to identify two instances of very tightly clustered sequences which we suggest are the results of global selective sweeps—one closely related to SCA1145, an abundant globally distributed group within the Terrestrial Group of Crenarchaeota, and another nested within the more basal FFSB group of sequences. We replicated our sequence results at two levels: first, by repeating the dilution and PCR processes from the same soil core DNA extraction, and second, by performing a replicate DNA extraction from the same homogenized soil core sample. Pairs of sequences produced by the dilution replicates were significantly more similar than the pairs of sequences produced by the extraction replicates, suggesting that soil Crenarchaeota exists in highly localized and discrete clonal populations.

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References

  1. Acinas, SG, Klepac-Ceraj, V, Hunt, DE, Pharino, C, Ceraj, I, Distel, DL, Polz, MF (2004) Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430: 551–554

    Article  PubMed  CAS  Google Scholar 

  2. Avise, JC (1994) Molecular Markers, Natural History, and Evolution. Chapman and Hall, New York

    Google Scholar 

  3. Barns, SM, Delwiche, CF, Palmer, JD, Pace, NR (1996) Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc Natl Acad Sci USA 93: 9188–9193

    Article  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. Borneman, J, Triplett, EW (1997) Molecular microbial diversity in soils from eastern Amazonia: evidence for unusual microorganisms and microbial population shifts associated with deforestation. Appl Environ Microbiol 63: 2647–2653

    PubMed  CAS  Google Scholar 

  6. 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 

  7. Cannone, JJ, Subramanian, S, Schnare, MN, Collett, JR, D'Souza, LM, Du, Y, Feng, B, Lin, N, Madabusi, LV, Muller, KM, Pande, N, Shang, Z, Yu, N, Gutell, RR (2002) The Comparative RNA Web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3: 2 [Correction: BioMed Central Bioinformatics. 3:15]

    Article  PubMed  Google Scholar 

  8. Chin, KJ, Lukow, T, Conrad, R (1999) Effect of temperature on structure and function of the methanogenic archaeal community in an anoxic rice field soil. Appl Environ Microbiol 65: 2341–2349

    PubMed  CAS  Google Scholar 

  9. Crump, BC, Baross, JA (2000) Archaeaplankton in the Columbia river, its estuary, and the adjacent coastal ocean, USA. FEMS Microbiol Ecol 31: 231–239

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  11. Felsenstein, J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368–376

    Article  PubMed  CAS  Google Scholar 

  12. Hershberger, KL, Barns, SM, Reysenbach, A, Dawson, SC, Pace, NR (1996) Wide diversity of Crenarchaeota. Nature 384: 420

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  14. Jurgens, G, Saano, A (1999) Diversity of soil Archaea in boreal forest before, and after clear-cutting and prescribed burning. FEMS Microb Ecol 29: 205–213

    CAS  Google Scholar 

  15. Lueders, T, Friedrich, MW (2000) Archaeal population dynamics during sequential reduction processes in rice field soil. Appl Environ Microbiol 66: 2732–2742

    Article  PubMed  CAS  Google Scholar 

  16. Majewski, J, Cohan, FM (1999) Adapt globally, act locally: the effect of selective sweeps on bacterial sequence diversity. Genetics 152: 1459–1474

    PubMed  CAS  Google Scholar 

  17. Marr, JW (1961) Ecosystems of the east slope of the Front Range in Colorado. Univ Colo Ser Biol, vol. 8. University of Colorado Press, Boulder, pp 1–134

  18. McInerney, JO, Wilkinson, M, Patching, JW, Embley, TM, Powell, R (1995) Recovery and phylogenetic analysis of novel archaeal rRNA sequences from a deep-sea deposit feeder. Appl Environ Microbiol 61: 1646–1648

    PubMed  CAS  Google Scholar 

  19. Miller, DN, Bryant, JE, Madsen, EL, Ghiorse, WC (1999) Evaluation and optimization of DNA extraction and purification procedures for soil and sediment samples. Appl Environ Microbiol 65: 4715–4724

    PubMed  CAS  Google Scholar 

  20. Moré, MI, Herrick, JB, Silva, MC, Ghiorse, WC, Madsen, EL (1994) Quantitative cell lysis of indigenous microorganisms and rapid extraction of microbial DNA from sediment. Appl Environ Microbiol 60: 1572–1580

    PubMed  Google Scholar 

  21. Nicol, GW, Glover, LA, Prosser, JL (2003) The impact of grassland management on archaeal community structure in upland pasture rhizosphere soil. Environ Microbiol 5: 152–162

    Article  PubMed  CAS  Google Scholar 

  22. Oline, DK, Grant, MC (2001) Scaling patterns of biomass and soil properties: an empirical analysis. Landscape Ecol 17: 13–26

    Article  Google Scholar 

  23. Olsen, GJ, Matsuda, H, Hagstrom, R, Overbeek, R (1994) fast DNAml: A tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci 10: 41–48

    PubMed  CAS  Google Scholar 

  24. Palys, T, Nakamura, LK, Cohan, FM (1997) Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int J Syst Bacteriol 47: 1145–1156

    Article  PubMed  CAS  Google Scholar 

  25. Qiu, X, Wu, L, Huang, H, McDonel, PE, Palumbo, AV, Tiedje, JM, Zhou, J (2001) Evaluation of PCR-generated chimeras, mutations, and heteroduplexes with 16S rRNA gene-based cloning. Appl Environ Microbiol 67(2): 880–887

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  27. Scala, DJ, Kerkhof, LJ (2000) Horizontal heterogeneity of denitrifying bacterial communities in marine sediments by terminal restriction fragment length polymorphism analysis. Appl Environ Microbiol 66: 1980–1986

    Article  PubMed  CAS  Google Scholar 

  28. Simon, HM, Dodsworth, JA, Goodman, RM (2000) Crenarchaeota colonize terrestrial plant roots. Environ Microbiol 2: 495–505

    Article  PubMed  CAS  Google Scholar 

  29. Sliwinski, MK, Goodman, RM (2004) Comparison of Crenarchaeal consortia inhabiting the rhizosphere of diverse terrestrial plants with those in bulk soil in native environments. Appl Environ Microbiol 70: 1821–1826

    Article  PubMed  CAS  Google Scholar 

  30. Vetriani, C, Jannasch, HW, MacGregor, BJ, Stahl, DA, Reysenbach, AL (1999) Population structure and phylogenetic characterization of marine benthic Archaea in deep-sea sediments. Appl Environ Microbiol 65: 4375–4384

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank J. Mitton, B. Kreiser, R. Ramey, A. Martin, T. Seastedt, and B. Bowman. We also thank the Arapahoe-Roosevelt National Forest, the University of Colorado Mountain Research Station, and the Niwot Ridge LTER site for their support. Thanks to R. Gutell for secondary structure diagrams of rRNA sequences, R. Sandaa for providing sequence data, and H. Simon for providing a preprint of her manuscript. Special thanks to samiam.colorado.edu for an outstanding effort devoted to the cause of molecular phylogeny.

Funding for this research was provided by the Colorado Mountain Club, the David Paddon Memorial Scholarship of the Indian Peaks Working Group, the Beverley Sears Deans Small Grants, Sigma Xi, the Department of EPO Biology at the University of Colorado, the National Science Foundation Dissertation Improvement Grants (DEB-9972713), and the Microbial Observatories program (DEB-0084243).

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Oline, D.K., Schmidt, S.K. & Grant, M.C. Biogeography and Landscape-Scale Diversity of the Dominant Crenarchaeota of Soil. Microb Ecol 52, 480–490 (2006). https://doi.org/10.1007/s00248-006-9101-5

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