Skip to main content

Advertisement

SpringerLink
Log in

The Community and Phylogenetic Diversity of Biological Soil Crusts in the Colorado Plateau Studied by Molecular Fingerprinting and Intensive Cultivation

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We studied the bacterial communities in biological soil crusts (BSCs) from the Colorado Plateau by enrichment and cultivation, and by statistically analyzed denaturing gradient gel electrophoresis (DGGE) fingerprinting of environmental 16S rRNA genes, and phylogenetic analyses. Three 500-m-long transects, tens of km apart, consisting of 10 equally spaced samples each, were analyzed. BSC communities consistently displayed less richness (10–32 detectable DGGE bands per sample) and Shannon diversity (2.1–3.3) than typical soil communities, with apparent dominance by few members. In spite of some degree of small-scale patchiness, significant differences in diversity and community structure among transects was detectable, probably related to the degree of crust successional maturity. Phylogenetic surveys indicated that the cyanobacterium Microcoleus vaginatus was dominant, with M. steenstrupii second among phototrophs. Among the 48 genera of nonphototrophs detected, Actinobacteria (particularly Streptomyces spp.) were very common and diverse, with 18 genera and an average contribution to the total 16S rDNA amplificate of 11.8%. β-Proteobacteria and Bacteriodetes contributed around 10% each; Low-GC Gram-positives, α-Proteobacteria, Thermomicrobiales, and Acidobacteria were common (2–5%). However, the second largest contribution was made by deep-branching unaffiliated alleles (12.6%), with some of them representing candidate bacterial divisions. Many of the novel strains isolated are likely new taxa, and some were representatives of the phylotypes detected in the field. The mucoid or filamentous nature of many of these isolates speaks for their role in crust formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Belnap, J, Gardner, JS (1993) Soil microstructure in soils of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus. Great Basin Nat 53: 40–47

    Google Scholar 

  2. Belnap, J, Lange, OL (Eds.) (2001) Biological Soil Crusts: Structure, Function, and Management, Vol. 150. Springer-Verlag, Berlin, Germany

    Google Scholar 

  3. Belnap, J (1994) Potential role of cryptobiotic soil crust in semiarid rangelands. In: Monsen, SB, Kitchen, SG (Eds.) Proceedings Ecology and Management of Annual Rangelands. USDA Forest Service. Intermountain Research Station, Ogden, UT, pp 179–185

    Google Scholar 

  4. Boyer, SL, Johansen, J, Flechtner, VR (2002) Phylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species on sequence analysis of the 16S rRNA gene and associated 16S–23S ITS region. J Phycol 38: 1222–1235

    Article  CAS  Google Scholar 

  5. Bowker, MA, Reed, SC , Belnap, J, Phillips, SL (2002) Temporal variation in community composition, pigmentation, and F v/F m of desert cyanobacterial soil crusts. Microb Ecol 43: 13–25

    Article  PubMed  CAS  Google Scholar 

  6. Buckley, DH, Schmidt, TM (2003) Diversity and dynamics of microbial communities in soils from agro-ecosystems. Environ Microbiol 5: 441–452

    Article  PubMed  Google Scholar 

  7. Don, RH, Cox, PT, Wainwright, B, Baker, K, Mattick, JS (1991) “Touchdown” PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19: 4008

    Article  PubMed  CAS  Google Scholar 

  8. Garcia-Pichel, F, Belnap, J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32: 774–782

    Article  Google Scholar 

  9. Garcia-Pichel, F, Belnap, J (2001) Microenvironments of biological soil crusts. In: Belnap, J, Lange, OL (Eds.) Biological soil crusts: structure, function and management. Springer-Verlag, Heidelberg

    Google Scholar 

  10. Garcia-Pichel, F, Lopez-Cortez, A, Nubel, U (2001) Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado Plateau. Appl Environ Microbiol 67: 1902–1910

    Article  PubMed  CAS  Google Scholar 

  11. Garcia-Pichel, F (2002) Desert environments: biological soil crusts. In: Bitton, G (Ed.) Encyclopedia of Environmental Microbiology. Wiley, New York

    Google Scholar 

  12. Garcia-Pichel, F, Johnson, SL, Youngkin, D, Belnap, J (2003) Small-scale vertical distribution of bacterial biomass and diversity in biological soil crusts from arid lands in the Colorado plateau. Microbial Ecol 46: 312–321

    Article  CAS  Google Scholar 

  13. Garcia-Pichel, F, Belnap, J, Neuer, S, Schanz, F (2003) Estimates of global cyanobacterial biomass and its distribution. Arch Hydrobiol/Algol Stud 109: 213–228

    Google Scholar 

  14. Hughes, KA, Lawley, B (2003) A novel Antarctic microbial endolithic community within gypsum crusts. Environ Microbiol 5: 555–565

    Article  PubMed  Google Scholar 

  15. Jackson, TJ, Ramaley, RF, Meinschein, WG (1973) Thermomicrobium, a new genus of extremely thermophilic bacteria. Int J Syst Bacteriol 23: 28–36

    Google Scholar 

  16. Jagannadham, MV, Chattopadhyay, MK, Shivaji, S (1996) The major carotenoid pigment of a psychrotrophic Micrococcus roseus strain: fluorescence properties of the pigment and its binding to membranes. Biochem Biophys Res Commun 220: 724–728

    Article  PubMed  CAS  Google Scholar 

  17. Johnson, SL, Charles, R, Budinoff, CR, Belnap, J, Garcia-Pichel, F (2005) Relevance of ammonium oxidation within biological soil crust communities. Environ Microbiol 7: 1–12

    Article  PubMed  CAS  Google Scholar 

  18. Joseph, SJ, Hugenholtz, P, Sangwan, P, Osborne, CA, Janssen, PH (2003) Laboratory cultivation of widespread and previously uncultured soil bacteria. Appl Environ Microbiol 69: 7210–7215

    Article  PubMed  CAS  Google Scholar 

  19. Kishimoto, N, Kosako, Y, Tano, T (1991) Acidobacterium capsulatum gen. nov., sp. nov.; an acidophilic chemoorganotrophic bacterium containing menaquinone from acidic mineral environment. Curr Microbiol 22: 1–7

    Article  CAS  Google Scholar 

  20. Kuske, CR, Ticknot, OL, Miller, ME, Dunbar, JM, Davis, JA, Barns, SM, Belnap, J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and interspaces in an arid grassland. Appl Environ Microbiol 68: 1854–1863

    Article  PubMed  CAS  Google Scholar 

  21. Kumar, SK, Tamura, IB, Jakobsen, IB, Nei, M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17: 1244–1245

    Article  PubMed  CAS  Google Scholar 

  22. Muyzer, G, Hottentrager, S, Teske, A, Wawer, C (1996) Denaturing gradient electrophoresis of PCR-amplified 16S rDNA: a new molecular approach to analyse the genetic diversity of mixed microbial communities. In: Akkermans, ADL, van Elsas, JD, de Bruijn, FJ (Eds.) Molecular Microbial Ecology Manual. Kluwer Academic Publishers, The Netherlands, pp 1–23(3.4.4)

    Google Scholar 

  23. Muyzer, G, de Waal, EC, Uitterlinden, AG (1993) Profiling of complex microbial populations by denaturing gradient electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695–700

    PubMed  CAS  Google Scholar 

  24. Muyzer, G, Teske, A, Wirsen, CO, Jannasch, HW (1995) Phylogenetic relationship of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164: 165–172

    Article  PubMed  CAS  Google Scholar 

  25. Nagy, M, Pérez, A, Garcia-Pichel, F (2005) The prokaryotic diversity of biological soil crusts in the Sonoran desert (Organ Pipe Cactus National Monument, AZ). FEMS Microbiol Ecol 54: 233–245

    Article  PubMed  CAS  Google Scholar 

  26. Nakatsua, CH, Torsvik, V, Øvreås, L (2000) Soil community analysis using DGGE of 16S rDNA polymerase chain reaction products. Soil Sci Soc Am J 64: 1382–1388

    Article  Google Scholar 

  27. Nogales, B, Moore, ER, Llobet-Brossa, E, Rossello-Mora, R, Amann, R, Timmis, KN (2001) Combined use of 16S ribosomal DNA and 16S rRNA to study the bacterial community of polychlorinated biphenyl-polluted soil. Appl Environ Microbiol 67: 1874–1884

    Article  PubMed  CAS  Google Scholar 

  28. Nübel, U, Garcia-Pichel, F, Muyzer, G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63: 3327–3332

    PubMed  Google Scholar 

  29. Nübel, U, Garcia-Pichel, F, Kühl, M, Muyzer, G (1999) Quantifying microbial diversity: morphotypes, 16S rRNA genes, and carotinoids of oxygenic phototrophs in microbial mats. Appl Environ Microbiol 65: 422–430

    PubMed  Google Scholar 

  30. Nubel, U, Garcia-Pichel, F, Clavero, E, Muyzer, G (2000) Matching molecular diversity and ecophysiology of benthic cyanobacteria and diatoms in communities along a salinity gradient. Environ Microbiol 2: 217–226

    Article  PubMed  CAS  Google Scholar 

  31. Purkhold, U, Wagner, M, Timmermann, G, Pommerening–Roser, A, Koops, HP (2003) 16S rRNA and amoA-based phylogeny of 12 novel betaproteobacterial ammonia-oxidizing isolates: extension of the dataset and proposal of a new lineage within the nitrosomonads. Int J Syst Evol Microbiol 53: 1485–1494

    Article  PubMed  CAS  Google Scholar 

  32. Rothrock, MJ, Garcia-Pichel, F (2005) Microbial diversity of benthic mats along a tidal desiccation gradient. Environ Microbiol 7: 593–601

    Article  PubMed  CAS  Google Scholar 

  33. Shannon, CE, Weaver, W (1949) The Mathematical Theory of Communication. University of Illinois Press, Urbana, IL

    Google Scholar 

  34. Smith, SM, Abed, RMM, Garcia-Pichel, F (2004) Biological soil crusts of sand dunes in Cape Cod National Seashore, Massachusetts, USA. Microbial Ecol 28: 200–208

    Article  CAS  Google Scholar 

  35. Stackebrandt, E, Goebel, BM (1994) Taxanomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44: 846–849

    Article  CAS  Google Scholar 

  36. Thompson, JD, Higgins, DG, Gibson, TJ (1994) CLUSTAL W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680

    Article  PubMed  CAS  Google Scholar 

  37. von Wintzingerode, F, Selent, B, Hegemann, W, Gobel, UB (1999) Phylogenetic analysis of an anaerobic, trichlorobenzene-transforming microbial consortium. Appl Environ Microbiol 65: 283–286

    Google Scholar 

  38. Wade, BD, Garcia-Pichel, F (2003) Evaluation of DNA extraction methods for molecular analyses of microbial communities in modern calcareous microbialites. Geomicrobiol J 20: 549–561

    Article  CAS  Google Scholar 

  39. Yeager, CM, Kornosky, JL, Housman, DC, Grote, EE, Belnap, J, Kuske, CR (2004) Diazotrophic community structure and function in two successional stages of biological soil crusts from the Colorado plateau and Chihuahuan desert. Appl Environ Microbiol 70: 973–983

    Article  PubMed  CAS  Google Scholar 

  40. Zhang, H, Sekiguchi, Y, Hanada, S, Hugenholtz, P, Kim, H, Kamagata, Y, Nakamura, K (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53: 1155–1163

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank A. Pérez, M. Nagy, and S. Johnson for help in the field DNA extraction. This research was funded by the National Science Foundation Biotic Surveys and Inventories grant 0206711 to Ferran Garcia-Pichel.

Author information

Authors and Affiliations

  1. School of Life Sciences (SoLS), Arizona State University, Tempe, AZ, 85287-4501, USA

    Sathyanarayana Reddy Gundlapally & Ferran Garcia-Pichel

Authors
  1. Sathyanarayana Reddy Gundlapally
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ferran Garcia-Pichel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ferran Garcia-Pichel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gundlapally, S.R., Garcia-Pichel, F. The Community and Phylogenetic Diversity of Biological Soil Crusts in the Colorado Plateau Studied by Molecular Fingerprinting and Intensive Cultivation. Microb Ecol 52, 345–357 (2006). https://doi.org/10.1007/s00248-006-9011-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9011-6

Keywords

Search

Navigation