Microbial Ecology

, Volume 46, Issue 3, pp 312–321 | Cite as

Small-Scale Vertical Distribution of Bacterial Biomass and Diversity in Biological Soil Crusts from Arid Lands in the Colorado Plateau

  • F. Garcia-Pichel
  • S. L. Johnson
  • D. Youngkin
  • J. Belnap


We characterized, at millimeter resolution, bacterial biomass, diversity, and vertical stratification of biological soil crusts in arid lands from the Colorado Plateau. Microscopic counts, extractable DNA, and plate counts of viable aerobic copiotrophs (VAC) revealed that the top centimeter of crusted soils contained atypically large bacterial populations, tenfold larger than those in uncrusted, deeper soils. The plate counts were not always consistent with more direct estimates of microbial biomass. Bacterial populations peaked at the immediate subsurface (1–2 mm) in light-appearing, young crusts, and at the surface (0–1 mm) in well-developed, dark crusts, which corresponds to the location of cyanobacterial populations. Bacterial abundance decreased with depth below these horizons. Spatially resolved DGGE fingerprints of Bacterial 16S rRNA genes demonstrated the presence of highly diverse natural communities, but we could detect neither trends with depth in bacterial richness or diversity, nor a difference in diversity indices between crust types. Fingerprints, however, revealed the presence of marked stratification in the structure of the microbial communities, probably a result of vertical gradients in physicochemical parameters. Sequencing and phylogenetic analyses indicated that most of the naturally occurring bacteria are novel types, with low sequence similarity (83–93%) to those available in public databases. DGGE analyses of the VAC populations indicated communities of lower diversity, with most types having sequences more than 94% similar to those in public databases. Our study indicates that soil crusts represent small-scale mantles of fertility in arid ecosystems, harboring vertically structured, little-known bacterial populations that are not well represented by standard cultivation methods.


Microbial Biomass Soil Crust Biological Soil Crust Desert Soil Colorado Plateau 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We gratefully acknowledge the technical help of Keith Varty, Christopher Eagle-Hawk, and Sasha Reed. This research was supported by grants from the US Department of Agriculture (NRI 35107-10054) and the National Science Foundation (BSI-0206711) to F.G.-P.


  1. 1.
    Bamforth, SS 1984Microbial distributions in Arizona deserts and woodlands.Soil Biol Biochem6133137CrossRefGoogle Scholar
  2. 2.
    Belnap, J, Gardner, JS 1993Soil microstructure in soils of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus.Great Basin Naturalist534047Google Scholar
  3. 3.
    Belnap, J, Lange, OL 2001Biological Soil Crusts: Structure, Function and Management, vol 1.Springer-VerlagBerlin503Google Scholar
  4. 4.
    Bolton Jr, H, Smith, JL, Link, SO 1993Soil microbial biomass and activity of a disturbed and undisturbed shrub-steppe ecosystem.Soil Biol Biochem25545552CrossRefGoogle Scholar
  5. 5.
    Boyer, SL, Johansen, JR, Flechtner, VR 2002Phylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species based on sequence analysis of the 16S rRNA gene and associated 16S–23S ITS region.J Phycol3812221235CrossRefGoogle Scholar
  6. 6.
    Campbell, CG, Ghodrati, M, Garrido, F 1999Comparison of time domain reflectometry, fiber optic mini-probes, and solution samplers for real time measurement of solute transport in soil.Soil Sci164156170CrossRefGoogle Scholar
  7. 7.
    Campbell, SE 1979Soil stabilization by a prokaryotic desert crust: implications for Precambrian land biota.Orig Life9335348PubMedGoogle Scholar
  8. 8.
    Colwell, FS 1989Microbiological comparison of surface soil and unsaturated subsurface soil from a semiarid high desert.Appl Environ Microbiol5524202423Google Scholar
  9. 9.
    de Winder, B, Pluis, J, Reus, LD, Mur, LR 1989Characterization of a cyanobacterial, algal dune crust in the coastal dunes in the Netherlands.Rosenberg, E eds. Microbial Mats: Physiological Ecology of Benthic Microbial Communitites,American Society for MicrobiologyWashington, DC7783Google Scholar
  10. 10.
    Don, RH, Cox, PT, Wainwright, B, Baker, K, Mattick, JS 1991“Touchdown” PCR to circumvent spurious priming during gene amplification.Nucleic Acids Res194008PubMedGoogle Scholar
  11. 11.
    Eldridge, DL, Greene, RSB 1994Microbiotic soil crusts: a review of their roles in soil and ecological processes in the rangelands of Australia.Aust J Soil Res32389415Google Scholar
  12. 12.
    Evans, RD, Johansen, JR 1999Microbiotic crusts and ecosystem processes.Crit Rev Plant Sci18183225CrossRefGoogle Scholar
  13. 13.
    Garcia-Moya, E, Kell, CMM 1970Contribution of shrubs to the nitrogen economy of a desert-wash plant community.Ecology518188Google Scholar
  14. 14.
    Garcia-Pichel, F 2002Desert Environments: Biological Soil Crusts.Bitton, G eds. Encyclopedia of Environmental Microbiology,John WileyNew York10191023Google Scholar
  15. 15.
    Garcia-Pichel, F, Belnap, J 1996Microenvironments and microscale productivity of cyanobacterial desert crusts.J Phycol32774782Google Scholar
  16. 16.
    Garcia-Pichel, F, Belnap, J 2001Small-scale environments and distribution of biological soils crusts.Lange, OL eds. Biological Soil Crusts: Structure, Function, and Management,Springer-VerlagBerlin193201Google Scholar
  17. 17.
    Garcia-Pichel, F, Belnap, J, Neuer, S, Schanz, F 2002Estimates of global cyanobacterial biomass and its distribution.Arch HydrobiolSuppl Alg Studies 119213228Google Scholar
  18. 18.
    Garcia-Pichel, F, Lopez-Cortez, A, Nübel, U 2001Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado Plateau.Appl Environ Microbiol6719021910CrossRefPubMedGoogle Scholar
  19. 19.
    Garcia-Pichel, F, Mechling, M, Castenholtz, RW 1994Diel migrations of microorganisms in a hypersaline microbial mat.Appl Environ Microbiol6015001511Google Scholar
  20. 20.
    Garcia-Pichel, F, Pringault, O 2001Cyanobacteria track water in desert soils.Nature413380381CrossRefPubMedGoogle Scholar
  21. 21.
    Garrity, GM, Heimbuch, BK, Gagliardi, M 1996Isolation of zoosporogenous actinomycetes from desert soils.J Indust Microbiol17260267Google Scholar
  22. 22.
    Herman, RP, Provencio, KR, Herrera-Matos, J, Torrez, RJ 1995Resource islands predict the distribution of heterotrophic bacteria in Chihuahuan desert soils.Apply Environ Microbiol6118161821Google Scholar
  23. 23.
    Holmes, AJ, Bowyer, J, Holley, MP, O’Donoghue, M, Montgomery, M, Gillings, MR 2000Diverse, yet-to-be-cultured members of the Rubrobacter subdivision of the Actinobacteria are widespread in Australian arid soils.FEMS Microbiol Ecol33111120CrossRefPubMedGoogle Scholar
  24. 24.
    Johansen, JR 1993Cryptogamic crusts of semiarid and arid lands of North America.J Phycol29140147Google Scholar
  25. 25.
    Karsten, U, Garcia-Pichel, F 1996Carotenoids and mycosporine-like amino acid compounds in members of the genus Microcoleus (Cyanobacteria): a chemosystematic study.System Appl Microbiol19285294Google Scholar
  26. 26.
    Kuske, CR, Barns, SM, Busch, JD 1997Diverse uncultivated bacterial groups from soils of the arid southwestern United States that are present in many geographic regions.Appl Environ Microbiol6336143621PubMedGoogle Scholar
  27. 27.
    Kuske, CR, Busch, JD, Adorada, DL, Dunbar, JM, Barns, SM 1999Phylogeny, ribosomal RNA gene typing and relative abundance of new Pseudomonas species (sensu stricto) isolated from two pinyon-juniper woodland soils of the arid southwest U.S. system.Appl Microbiol22300311Google Scholar
  28. 28.
    Kuske, CR, Ticknor, LO, Miller, ME, Dunbar, JM, Davis, JA, Barns, SM, Belnap, J 2002Comparison of soil bacterial communitites in rhizospheres of three plant species and the interspaces in an arid grassland.Appl Environ Microbiol6818541863Google Scholar
  29. 29.
    Lorch, HJ, Beckiser, G, Ottow, JCG 1995Basic methods for counting microorganisms in soil and water.Nannipieri, KAAP eds. Methods in Applied Soil Microbiology and Biochemistry,Academic PressSan Diego162170Google Scholar
  30. 30.
    Muyzer, G, Teske, A, Wirsen, CO, Jannasch, HW 1995Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments.Arch Microbiol164165172CrossRefPubMedGoogle Scholar
  31. 31.
    Nübel, U, Garcia-Pichel, F, Kuhl, M, Muyzer, G 1999Quantifying microbial diversity: morphotypes, 16S rRNA genes, carotenoids of oxygenic phototrophs in microbial mats.Appl Environ Microbiol65422430PubMedGoogle Scholar
  32. 32.
    Ranjard, L, Poly, F, Combrisson, J, Richaume, A, Gourbiere, F, Thioulouse, J, Nazaret, S 2000Heterogenous cell density and genetic structure of bacterial pools associated with various soil microenvironments as determined by enumeration and DNA fingerprinting approach (RISA).Microb Ecol39263272PubMedGoogle Scholar
  33. 33.
    Roberts, MS, Nakamura, LK, Cohan, FM 1994 Bacillus mojavensis sp. nov., distinguishable from Bacillus subtillis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition.Int J Syst Evol Microbiol44256264Google Scholar
  34. 34.
    Schramm, A, DeBeer, D, Gieseke, A, Amann, R 2000Microenvironments and distribution of nitrifying bacteria in a membrane-bound biofilm.Environ Microbiol2680686CrossRefPubMedGoogle Scholar
  35. 35.
    Schulten, JA 1985Soil aggregation by cryptogams of a sand prairie.Am J Bot7216571661Google Scholar
  36. 36.
    Tan, ZY, Kan, FL, Peng, GX, Wang, ET, Reinhold-Hurek, B, Chen, WX 2001 Rhizobium yanglingense sp. nov., isolated from arid and semi-arid regions in China.Int J Syst Evol Microbiol51909914PubMedGoogle Scholar
  37. 37.
    Tankéré, SPC, Bourne, DG, Muller, FLL, Torsvik, V 2002Microenvironments and microbial community structure in sediments.Environ Microbiol497106CrossRefPubMedGoogle Scholar
  38. 38.
    Taylor, JP, Wilson, B, Mills, MS, Burns, RG 2002Comparison of microbial numbers and enzymatic activities in suface soils and subsoils using various techniques.Soil Biol Biochem34387401CrossRefGoogle Scholar
  39. 39.
    Wade, B, Garcia-Pichel, F 2002Evaluation of DNA extraction methods for molecular analysis of microbial communities in modern microbialites.Geomicrobiology(in press)Google Scholar
  40. 40.
    West, NE 1990Structure and function of soil microphytic crusts in wildland ecosystems of arid and semi-arid regions.Adv Ecol Res20179223Google Scholar
  41. 41.
    Wynn-Williams, DD 1985Photofading retardant for epiflourescence microscopy in soil micro-ecological studies.Soil Biol Biochem17739746CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • F. Garcia-Pichel
    • 1
  • S. L. Johnson
    • 1
  • D. Youngkin
    • 1
  • J. Belnap
    • 2
  1. 1.Microbiology DepartmentArizona State University, Tempe, AZ 85287USA
  2. 2.US Geological Survey, 2290 West Resource Blvd., Moab, UT 84532USA

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