Skip to main content

Advertisement

SpringerLink
Log in

Analyses of dryland biological soil crusts highlight lichens as an important regulator of microbial communities

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Biological soil crusts (BSCs) provide important ecosystem services in dryland regions, including erosion control and contribution to nitrogen and CO2 fixation. As soil microorganisms are still rarely studied within the context of biodiversity planning, we describe, as a contribution to the Soil Crust International project, an approach that addresses this gap in biodiversity assessments. The purpose of the present study was a characterization of prokaryotic communities of BSCs formed by two species of lichenized fungi, Psora decipiens and Toninia sedifolia, in relation to surrounding BSCs and the below-crust soil layer from Tabernas basin (Almería, Spain). Microbial community profiles were determined using 454 pyrosequencing targeting the V4 hypervariable region of the bacterial and archaeal 16S rRNA gene. The majority of the 65,497 sequences obtained belonged to Proteobacteria (mainly Alphaproteobacteria), Actinobacteria, Bacteroidetes and Cyanobacteria. Cyanobacteria were more abundant at the soil surface but rare in below-crust soils, whilst below-crust soils harbored significantly more Acidobacteria, Verrucomicrobia, Gemmatimonadetes, Planctomycetes and Armatimonadetes. Additionally, terricolous lichens were investigated using fluorescence in situ hybridization in conjunction with confocal laser scanning microscopy, the objective being to illustrate bacterial niches in BSC-forming lichens. Bacteria were mainly present at the upper cortex of the squamules and attachment organs. Our findings indicate that the composition of soil prokaryotes varies at a small scale not only in adjacent soil layers but also in BSC-forming lichen species. Furthermore, bacteria were shown to be attached to fungal structures, probably representing a case of fungal-bacterial interaction.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abed RMM, Kharusi SA, Schramm A, Robinson MD (2010) Bacterial diversity, pigments and nitrogen fixation of biological desert crusts from the Sultanate of Oman. FEMS Microbiol Ecol 72:418–428

    Article  CAS  PubMed  Google Scholar 

  • Adeel Z (2008) Findings of the global desertification assessment by the millenium ecosystem assessment—a perspective for better managing scientific knowledge. In: Lee C, Schaaf T (eds) The future of drylands. Springer, Netherlands, pp 677–685

    Google Scholar 

  • Amann R, Fuchs BM (2008) Single-cell identification in microbial communities by improved fluorescence in situ hybridization techniques. Nature Rev Microbiol 6:339–348

    Article  CAS  Google Scholar 

  • Barger NN, Herrick JE, Van Zee J, Belnap J (2006) Impacts of biological soil crust disturbance and composition on c and n loss from water erosion. Biogeochemistry 77:247–263

    Article  CAS  Google Scholar 

  • Bates ST, Cropsey GW, Caporaso JG, Knight R (2011a) Bacterial communities associated with the lichen symbiosis. Appl Environ Microbiol 77:1309–1314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bates ST, Berg-Lyons D, Caporaso JG, Walters WA et al (2011b) Examining the global distribution of dominant archaeal populations in soil. ISME J 5:908–917

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Belnap J (2003) The world at your feet: desert biological soil crusts. Front Ecol Environ 1:181–189

    Article  Google Scholar 

  • Belnap J, Eldridge D (2003) Disturbance and recovery of biological soil crusts. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management, ecological studies, vol 150. Springer, Berlin, pp 363–383

    Chapter  Google Scholar 

  • Belnap J, Lange OL (2003) Biological soil crusts: structure, function, and management. In: Baldwin IT, Caldwell MM, Heldmaier G, Lange OL, Mooney HA, Schulze ED, Sommer U (eds) Ecological studies series 150, vol 150. Springer, Berlin

    Google Scholar 

  • Bjelland T, Grube M, Hoem S, Jorgensen SL et al (2011) Microbial metacommunities in the lichen-rock habitat. Environ Microbiol Rep 3:434–442

    Article  PubMed  Google Scholar 

  • Büdel B (2003) Biological soil crusts in European temperate and mediterranean regions. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management, ecological studies, vol 150. Springer, Berlin, pp 75–87

    Chapter  Google Scholar 

  • Büdel B, Colesie C, Allan Green TG, Grube M et al (2014) Improved appreciation of the functioning and importance of biological soil crusts in Europe: the Soil Crust International Project (SCIN). Biodivers Conserv. doi:10.1007/s10531-014-0645-2

    Google Scholar 

  • Cantón Y, Del Barrio G, Solé-Benet A, Lázaro R (2004) Topographic controls on the spatial distribution of ground cover in the Tabernas badlands of SE Spain. Catena 55:341–365

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K et al (2011) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  Google Scholar 

  • Cardinale M, Puglia AM, Grube M (2006) Molecular analysis of lichen-associated bacterial communities. FEMS Microbiol Ecol 57:484–495

    Article  CAS  PubMed  Google Scholar 

  • Cardinale M, Castro JV Jr, Müller H, Berg G, Grube M (2008) In situ analysis of the bacterial community associated with the reindeer lichen Cladonia arbuscula reveals predominance of Alphaproteobacteria. FEMS Microbiol Ecol 66:63–71

    Article  CAS  PubMed  Google Scholar 

  • Cardinale M, Grube M, Berg G (2011) Frondihabitans cladoniiphilus sp., an actinobcterium of the family Microbacteriaceae isolated from lichen, and emended description of the genus Frondihabitans. Int J Syst Evol Microbiol 61:3033–3038

    Article  CAS  PubMed  Google Scholar 

  • Castillo-Monroy AP, Bowker MA, Maestre FT, Rodríguez-Echeverría S et al (2011) Relationships between biological soil crusts, bacterial diversity and abundance, and ecosystem functioning: insights from a semi-arid Mediterranean environment. J Veg Sci 22:165–174

    Article  Google Scholar 

  • Chau JF, Bagtzoglou AC, Willig MR (2011) The effect of soil texture on richness and diversity of bacterial communities. Environ Forensics 12:333–341

    Article  CAS  Google Scholar 

  • Csotonyi JT, Swiderski J, Stackebrandt E, Yurkov V (2010) A new environment for aerobic anoxygenic phototrophic bacteria: biological soil crusts. Environ Microbiol Rep 2:651–656

    Article  CAS  PubMed  Google Scholar 

  • Daims H (2009) Use of fluorescence in situ hybridization and the daime image analysis program for the cultivation-independent quantification of microorganisms in environmental and medical samples. Cold Spring Harb Protoc. doi:10.1101/pdb.prot5253

    PubMed  Google Scholar 

  • Daims H, Brühl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444

    Article  CAS  PubMed  Google Scholar 

  • Demoling F, Figueroa D, Bååth E (2007) Comparison of factors limiting bacterial growth in different soils. Soil Biol Biochem 39:2485–2495

    Article  CAS  Google Scholar 

  • Dojani S, Büdel B, Deutschewitz K, Weber B (2011) Rapid succession of biological soil crusts after experimental disturbance in the succulent karoo, South Africa. App Soil Ecol 48:263–269

    Article  Google Scholar 

  • Dunkel FG (2003) Die Karlstadter Trockenrasen. Ein Pflanzenführer zu international bedeutsamen Magerrasen. Regierung von Unterfranken, Würzburg

    Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Elbert W, Weber B, Büdel B, Andreae MO, Pöschl U (2009) Microbiotic crusts on soil, rock and plants: neglected major players in the global cycles of carbon and nitrogen? Biogeosci Discuss 6:6983–7015

    Article  Google Scholar 

  • Elbert W, Weber B, Burrows S, Steinkamp J (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:1–4

    Article  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Göransson H, Venterink HO, Bååth E (2011) Soil bacterial growth and nutrient limitation along a chronosequence from a glacier forefield. Soil Biol Biochem 43:1333–1340

    Article  Google Scholar 

  • Griffiths RI, Thomson BC, James P, Bell T et al (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654

    Article  PubMed  Google Scholar 

  • Grube M, Cardinale M, Castro JV Jr, Müller H (2009) Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J 3:1105–1115

    Article  PubMed  Google Scholar 

  • Gundlapally SR, Garcia-Pichel F (2006) The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microbiol Ecol 52:345–357

    Article  Google Scholar 

  • Hodkinson BP, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180

    Article  CAS  Google Scholar 

  • Hodkinson BP, Neil RG, Schadt CW, Lutzoni F (2012) Photoautotrophic symbiont and geography are major factors affecting highly structured and diverse bacterial communities in the lichen microbiome. Environ Microbiol 14:147–161

    Article  CAS  PubMed  Google Scholar 

  • Johnson SL, Garcia-Pichel F, 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. Microb Ecol 46:312–321

    Article  PubMed  Google Scholar 

  • Köberl M, Müller H, Ramadan EM, Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PloS ONE 6:e24452–e24452. doi:10.1371/journal.pone.0024452

    Article  PubMed Central  PubMed  Google Scholar 

  • Kuske CR, Ticknor LO, Miller ME, Dunbar JM et al (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68:1854–1863

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kuske CR, Yeager CM, Johnson S, Ticknor LO, Belnap J (2012) Response and resilience of soil biocrust bacterial communities to chronic physical disturbance in arid shrublands. ISME J 6:886–897

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Langhans TM, Storm C, Schwabe A (2009) Community assembly of biological soil crusts of different successional stages in a temperate sand ecosystem, as assessed by direct determination and enrichment techniques. Microb Ecol 58:394–407

    Article  PubMed  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Loy A, Maixner F, Wagner M, Horn M (2007) probeBase—an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res. doi:10.1093/nar/gkl856

    PubMed Central  PubMed  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac : a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. ISME J 5:169–172

    Article  PubMed Central  PubMed  Google Scholar 

  • Maestre FT, Bowker MA, Cantón Y, Castillo-Monroy AP et al (2011) Ecology and functional roles of biological soil crusts in semi-arid ecosystems of Spain. J Arid Environ 75:1282–1291

    Article  Google Scholar 

  • Matias Rodrigues JF, von Mering (2014) HPC-CLUST: distributed hierarchical clustering for large sets of nucleotide sequences. Bioinformatics 30:287–288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moquin SA, Garcia JR, Brantley SL, Takacs-Vesbach CD et al (2012) Bacterial diversity of bryophyte-dominant biological soil crusts and associated mites. J Arid Environ 87:110–117

    Article  Google Scholar 

  • Muggia L, Klub B, Berg G, Grube M (2013) Localization of bacteria in lichens from Alpine soil crusts by fluorescence in situ hybridization. Appl Soil Ecol 68:20–25

    Article  Google Scholar 

  • Nagy ML, Garcia-Pichel F, Pérez A (2005) The prokaryotic diversity of biological soil crusts in the Sonoran Desert (Organ Pipe Cactus National Monument, AZ). FEMS Microbiol Ecol 54:33–245

    Article  Google Scholar 

  • Nawrocki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25:1335–1337

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P et al (2013) Vegan: community ecology package. http://cran.r-project.org/web/packages/vegan/vegan.pdf. Accessed 1 Aug 2013

  • Parker SS (2010) Buried treasure: soil biodiversity and conservation. Biodivers Conserv 19:3743–3756

    Article  Google Scholar 

  • Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562

    Article  CAS  PubMed  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. doi:10.1371/journal.pone.0009490

    Article  PubMed Central  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 1 Jan 2013

  • Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schneider T, Schmid E, de Castro JV, Jr Cardinale M et al (2011) Structure and function of the symbiosis partners of the lung lichen (Lobaria pulmonaria L. Hoffm.) analyzed by metaproteomics. Proteomics 11:2752–2756

    Article  CAS  PubMed  Google Scholar 

  • Schüller H (1969) Die CAL-Methode, eine neue Methode zur Bestimmung des pflanzenverfügbaren Phosphates in Böden. Z Pflanzenernähr Bodenkd 123:48–63

    Article  Google Scholar 

  • Sessitsch A, Weilharter A, Gerzabek MH, Kirchmann H, Kandeler E (2001) Microbial population structures in soil particle size fractions of a long-term fertilizer field experiment. Appl Environ Microbiol 67:4215–4224

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Soule T, Anderson IJ, Johnson SL, Bates ST et al (2009) Archaeal populations in biological soil crusts from arid lands in North America. Soil Biol Biochem 41:2069–2074

    Article  CAS  Google Scholar 

  • Souza-Egipsy V, Ascaso C, Sancho LG (2002) Water distribution within terricolous lichens revealed by scanning electron microscopy and its relevance in soil crust ecology. Mycol Res 106:1367–1374

    Article  Google Scholar 

  • Spain AM, Krumholz LR, Elshahed MS (2009) Abundance, composition, diversity and novelty of soil Proteobacteria. ISME J 3:992–1000

    Article  CAS  PubMed  Google Scholar 

  • Stark M, Berger SA, Stamatakis A, von Mering C (2010) MLTreeMap—accurate Maximum Likelihood placement of environmental DNA sequences into taxonomic and functional reference phylogenies. BMC Genom 11:461–471

    Article  Google Scholar 

  • Steven B, Gallegos-Graves LV, Belnap J, Kuske CR (2013) Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material. FEMS Microbiol Ecol 86:1–13

    Article  Google Scholar 

  • Visconti F, de Paz JM, Rubio JL (2010) What information does the electrical conductivity of soil water extracts of 1 to 5 ratio (w/v) provide for soil salinity assessment of agricultural irrigated lands? Geoderma 154:387–397

    Article  CAS  Google Scholar 

  • Wallner G, Amann R, Beisker W (1993) Optimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14:136–143

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Warmink JA, Nazir R, van Elsas JD (2009) Universal and species-specific bacterial “fungiphiles” in the mycospheres of different basidiomycetous fungi. Environ Microbiol 11:300–312

    Article  CAS  PubMed  Google Scholar 

  • White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5:e1000352. doi:10.1371/journal.pcbi.1000352

    Article  PubMed Central  PubMed  Google Scholar 

  • Yeager CM, Kornosky JL, Housman DC, Grote EE et al (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  CAS  PubMed Central  PubMed  Google Scholar 

  • Zarda B, Hahn D, Chatzinotas A, Schönhuber W et al (1997) Analysis of bacterial community structure in bulk soil by in situ hybridization. Arch Microbiol 168:185–192

    Article  CAS  Google Scholar 

  • Zhang B, Zhang Y, Downing A, Niu Y (2011) Distribution and composition of cyanobacteria and microalgae associated with biological soil crusts in the Gurbantunggut Desert, China. Arid Land Res Manag. doi:10.1080/15324982.2011.565858

Download references

Acknowledgments

This research was funded by the ERA-Net BiodivERsA, with the national funder Austrian Science Foundation (Fonds zur Förderung der wissenschaftlichen Forschung; FWF-1799), part of the 2011 BiodivERsA call for research proposals. We would like to thank La Estación Experimental de Zonas Áridas, particularly Dr. Roberto Lázaro Suau, for allowing us to use their laboratory facilities. We wish to thank two anonymous reviewers for constructive comments that greatly improved the quality of the manuscript. We express our thanks to Toby Spribille, Ines A. Aschenbrenner and Barbara Klug, for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. Institute of Plant Sciences, University of Graz, Graz, Austria

    Stefanie Maier, Viktoria Wagner & Martin Grube

  2. Bioinformatics Group, Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland

    Thomas S. B. Schmidt

  3. Department of Organismic Biology, University of Salzburg, Salzburg, Austria

    Lingjuan Zheng & Thomas Peer

  4. Department of Botany and Zoology, Masaryk University, Brno, Czech Republic

    Viktoria Wagner

Authors
  1. Stefanie Maier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas S. B. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lingjuan Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas Peer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Viktoria Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Martin Grube
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefanie Maier.

Additional information

Communicated by Guest Editors of S.I.: Biocrust.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 227 kb)

Supplementary material 2 (PDF 6023 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maier, S., Schmidt, T.S.B., Zheng, L. et al. Analyses of dryland biological soil crusts highlight lichens as an important regulator of microbial communities. Biodivers Conserv 23, 1735–1755 (2014). https://doi.org/10.1007/s10531-014-0719-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-014-0719-1

Keywords

Search

Navigation