Skip to main content
SpringerLink
Log in

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

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

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.

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

Similar content being viewed by others

References

  1. SS Bamforth (1984) ArticleTitleMicrobial distributions in Arizona deserts and woodlands. Soil Biol Biochem 6 133–137 Occurrence Handle10.1016/0038-0717(84)90103-2

    Article  Google Scholar 

  2. J Belnap JS Gardner (1993) ArticleTitleSoil microstructure in soils of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus. Great Basin Naturalist 53 40–47

    Google Scholar 

  3. J Belnap OL Lange (2001) Biological Soil Crusts: Structure, Function and Management, vol 1. Springer-Verlag Berlin 503

    Google Scholar 

  4. H Bolton Jr JL Smith SO Link (1993) ArticleTitleSoil microbial biomass and activity of a disturbed and undisturbed shrub-steppe ecosystem. Soil Biol Biochem 25 545–552 Occurrence Handle10.1016/0038-0717(93)90192-E

    Article  Google Scholar 

  5. SL Boyer JR Johansen VR Flechtner (2002) ArticleTitlePhylogeny and genetic variance in terrestrial Microcoleus (Cyanophyceae) species based on sequence analysis of the 16S rRNA gene and associated 16S–23S ITS region. J Phycol 38 1222–1235 Occurrence Handle10.1046/j.1529-8817.2002.01168.x Occurrence Handle1:CAS:528:DC%2BD3sXms1ahtg%3D%3D

    Article  CAS  Google Scholar 

  6. CG Campbell M Ghodrati F Garrido (1999) ArticleTitleComparison of time domain reflectometry, fiber optic mini-probes, and solution samplers for real time measurement of solute transport in soil. Soil Sci 164 156–170 Occurrence Handle10.1097/00010694-199903000-00002 Occurrence Handle1:CAS:528:DyaK1MXitFylsr0%3D

    Article  CAS  Google Scholar 

  7. SE Campbell (1979) ArticleTitleSoil stabilization by a prokaryotic desert crust: implications for Precambrian land biota. Orig Life 9 335–348 Occurrence Handle1:CAS:528:DyaL3cXjs1Chsg%3D%3D Occurrence Handle116183

    CAS  PubMed  Google Scholar 

  8. FS Colwell (1989) ArticleTitleMicrobiological comparison of surface soil and unsaturated subsurface soil from a semiarid high desert. Appl Environ Microbiol 55 2420–2423

    Google Scholar 

  9. B de Winder J Pluis LD Reus LR Mur (1989) Characterization of a cyanobacterial, algal dune crust in the coastal dunes in the Netherlands. E Rosenberg (Eds) Microbial Mats: Physiological Ecology of Benthic Microbial Communitites, American Society for Microbiology Washington, DC 77–83

    Google Scholar 

  10. RH Don PT Cox B Wainwright K Baker JS Mattick (1991) ArticleTitle“Touchdown” PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res 19 4008 Occurrence Handle1:CAS:528:DyaK3MXmtVShu70%3D Occurrence Handle1861999

    CAS  PubMed  Google Scholar 

  11. DL Eldridge RSB Greene (1994) ArticleTitleMicrobiotic soil crusts: a review of their roles in soil and ecological processes in the rangelands of Australia. Aust J Soil Res 32 389–415

    Google Scholar 

  12. RD Evans JR Johansen (1999) ArticleTitleMicrobiotic crusts and ecosystem processes. Crit Rev Plant Sci 18 183–225 Occurrence Handle10.1016/S0735-2689(99)00384-6

    Article  Google Scholar 

  13. E Garcia-Moya CMM Kell (1970) ArticleTitleContribution of shrubs to the nitrogen economy of a desert-wash plant community. Ecology 51 81–88

    Google Scholar 

  14. F Garcia-Pichel (2002) Desert Environments: Biological Soil Crusts. G Bitton (Eds) Encyclopedia of Environmental Microbiology, John Wiley New York 1019–1023

    Google Scholar 

  15. F Garcia-Pichel J Belnap (1996) ArticleTitleMicroenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32 774–782

    Google Scholar 

  16. F Garcia-Pichel J Belnap (2001) Small-scale environments and distribution of biological soils crusts. OL Lange (Eds) Biological Soil Crusts: Structure, Function, and Management, Springer-Verlag Berlin 193–201

    Google Scholar 

  17. F Garcia-Pichel J Belnap S Neuer F Schanz (2002) ArticleTitleEstimates of global cyanobacterial biomass and its distribution. Arch Hydrobiol Suppl Alg Studies 119 213–228

    Google Scholar 

  18. F Garcia-Pichel A Lopez-Cortez U Nübel (2001) ArticleTitlePhylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado Plateau. Appl Environ Microbiol 67 1902–1910 Occurrence Handle10.1128/AEM.67.4.1902-1910.2001 Occurrence Handle1:CAS:528:DC%2BD3MXis1egur4%3D Occurrence Handle11282648

    Article  CAS  PubMed  Google Scholar 

  19. F Garcia-Pichel M Mechling RW Castenholtz (1994) ArticleTitleDiel migrations of microorganisms in a hypersaline microbial mat. Appl Environ Microbiol 60 1500–1511

    Google Scholar 

  20. F Garcia-Pichel O Pringault (2001) ArticleTitleCyanobacteria track water in desert soils. Nature 413 380–381 Occurrence Handle10.1038/35096640 Occurrence Handle1:CAS:528:DC%2BD3MXntl2htbg%3D Occurrence Handle11574875

    Article  CAS  PubMed  Google Scholar 

  21. GM Garrity BK Heimbuch M Gagliardi (1996) ArticleTitleIsolation of zoosporogenous actinomycetes from desert soils. J Indust Microbiol 17 260–267 Occurrence Handle1:CAS:528:DyaK2sXltF2mug%3D%3D

    CAS  Google Scholar 

  22. RP Herman KR Provencio J Herrera-Matos RJ Torrez (1995) ArticleTitleResource islands predict the distribution of heterotrophic bacteria in Chihuahuan desert soils. Apply Environ Microbiol 61 1816–1821 Occurrence Handle1:CAS:528:DyaK2MXlsFykt7w%3D

    CAS  Google Scholar 

  23. AJ Holmes J Bowyer MP Holley M O’Donoghue M Montgomery MR Gillings (2000) ArticleTitleDiverse, yet-to-be-cultured members of the Rubrobacter subdivision of the Actinobacteria are widespread in Australian arid soils. FEMS Microbiol Ecol 33 111–120 Occurrence Handle10.1016/S0168-6496(00)00051-9 Occurrence Handle1:CAS:528:DC%2BD3cXmtVCrurk%3D Occurrence Handle10967210

    Article  CAS  PubMed  Google Scholar 

  24. JR Johansen (1993) ArticleTitleCryptogamic crusts of semiarid and arid lands of North America. J Phycol 29 140–147

    Google Scholar 

  25. U Karsten F Garcia-Pichel (1996) ArticleTitleCarotenoids and mycosporine-like amino acid compounds in members of the genus Microcoleus (Cyanobacteria): a chemosystematic study. System Appl Microbiol 19 285–294

    Google Scholar 

  26. CR Kuske SM Barns JD Busch (1997) ArticleTitleDiverse uncultivated bacterial groups from soils of the arid southwestern United States that are present in many geographic regions. Appl Environ Microbiol 63 3614–3621 Occurrence Handle1:CAS:528:DyaK2sXmtVKhtbY%3D Occurrence Handle9293013

    CAS  PubMed  Google Scholar 

  27. CR Kuske JD Busch DL Adorada JM Dunbar SM Barns (1999) ArticleTitlePhylogeny, 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 Microbiol 22 300–311 Occurrence Handle1:STN:280:DyaK1MzhvFemsA%3D%3D

    CAS  Google Scholar 

  28. CR Kuske LO Ticknor ME Miller JM Dunbar JA Davis SM Barns J Belnap (2002) ArticleTitleComparison of soil bacterial communitites in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68 1854–1863

    Google Scholar 

  29. HJ Lorch G Beckiser JCG Ottow (1995) Basic methods for counting microorganisms in soil and water. KAAP Nannipieri (Eds) Methods in Applied Soil Microbiology and Biochemistry, Academic Press San Diego 162–170

    Google Scholar 

  30. G Muyzer A Teske CO Wirsen HW Jannasch (1995) ArticleTitlePhylogenetic relationships 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 Occurrence Handle10.1007/s002030050250 Occurrence Handle1:CAS:528:DyaK2MXovFyjsrk%3D Occurrence Handle7545384

    Article  CAS  PubMed  Google Scholar 

  31. U Nübel F Garcia-Pichel M Kuhl G Muyzer (1999) ArticleTitleQuantifying microbial diversity: morphotypes, 16S rRNA genes, carotenoids of oxygenic phototrophs in microbial mats. Appl Environ Microbiol 65 422–430 Occurrence Handle9925563

    PubMed  Google Scholar 

  32. L Ranjard F Poly J Combrisson A Richaume F Gourbiere J Thioulouse S Nazaret (2000) ArticleTitleHeterogenous cell density and genetic structure of bacterial pools associated with various soil microenvironments as determined by enumeration and DNA fingerprinting approach (RISA). Microb Ecol 39 263–272 Occurrence Handle1:CAS:528:DC%2BD3cXlsFGhtLc%3D Occurrence Handle10882431

    CAS  PubMed  Google Scholar 

  33. MS Roberts LK Nakamura FM Cohan (1994) ArticleTitle 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 Microbiol 44 256–264 Occurrence Handle1:CAS:528:DyaK2cXlsFeitbo%3D

    CAS  Google Scholar 

  34. A Schramm D DeBeer A Gieseke R Amann (2000) ArticleTitleMicroenvironments and distribution of nitrifying bacteria in a membrane-bound biofilm. Environ Microbiol 2 680–686 Occurrence Handle10.1046/j.1462-2920.2000.00150.x Occurrence Handle1:STN:280:DC%2BD3M7otVWksg%3D%3D Occurrence Handle11214800

    Article  CAS  PubMed  Google Scholar 

  35. JA Schulten (1985) ArticleTitleSoil aggregation by cryptogams of a sand prairie. Am J Bot 72 1657–1661

    Google Scholar 

  36. ZY Tan FL Kan GX Peng ET Wang B Reinhold-Hurek WX Chen (2001) ArticleTitle Rhizobium yanglingense sp. nov., isolated from arid and semi-arid regions in China. Int J Syst Evol Microbiol 51 909–914 Occurrence Handle1:CAS:528:DC%2BD3MXks1Kiu78%3D Occurrence Handle11411714

    CAS  PubMed  Google Scholar 

  37. SPC Tankéré DG Bourne FLL Muller V Torsvik (2002) ArticleTitleMicroenvironments and microbial community structure in sediments. Environ Microbiol 4 97–106 Occurrence Handle10.1046/j.1462-2920.2002.00274.x Occurrence Handle11972619

    Article  PubMed  Google Scholar 

  38. JP Taylor B Wilson MS Mills RG Burns (2002) ArticleTitleComparison of microbial numbers and enzymatic activities in suface soils and subsoils using various techniques. Soil Biol Biochem 34 387–401 Occurrence Handle10.1016/S0038-0717(01)00199-7 Occurrence Handle1:CAS:528:DC%2BD38XhtVKns7g%3D

    Article  CAS  Google Scholar 

  39. B Wade F Garcia-Pichel (2002) ArticleTitleEvaluation of DNA extraction methods for molecular analysis of microbial communities in modern microbialites. Geomicrobiology Occurrence Handle1:CAS:528:DC%2BD38Xit1Wgtbw%3D

    CAS  Google Scholar 

  40. NE West (1990) ArticleTitleStructure and function of soil microphytic crusts in wildland ecosystems of arid and semi-arid regions. Adv Ecol Res 20 179–223

    Google Scholar 

  41. DD Wynn-Williams (1985) ArticleTitlePhotofading retardant for epiflourescence microscopy in soil micro-ecological studies. Soil Biol Biochem 17 739–746 Occurrence Handle10.1016/0038-0717(85)90127-0

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Microbiology Department, Arizona State University, Tempe, AZ 85287, USA

    F. Garcia-Pichel, S. L. Johnson & D. Youngkin

  2. US Geological Survey, 2290 West Resource Blvd., Moab, UT 84532, USA

    J. Belnap

Authors
  1. F. Garcia-Pichel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. L. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Youngkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Belnap
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. Garcia-Pichel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garcia-Pichel, F., Johnson, S., Youngkin, D. et al. Small-Scale Vertical Distribution of Bacterial Biomass and Diversity in Biological Soil Crusts from Arid Lands in the Colorado Plateau . Microb Ecol 46, 312–321 (2003). https://doi.org/10.1007/s00248-003-1004-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-003-1004-0

Keywords

Search

Navigation