Skip to main content
SpringerLink
Log in

Bacteria and Non-lichenized Fungi Within Biological Soil Crusts

  • Chapter
  • First Online:
Biological Soil Crusts: An Organizing Principle in Drylands

Part of the book series: Ecological Studies ((ECOLSTUD,volume 226))

Abstract

Biological soil crusts (biocrusts) are found in a broad range of climatic zones as components of open vegetation. In addition to photosynthetically active and N-fixing Cyanobacteria, heterotrophic bacteria and fungi are integral components of biocrusts. In this chapter, we present an overview of the diversity and interactions of fungi and bacteria. Both can occur “free-living” or in tight associations. Lichen symbioses, which frequently form a dominating aspect of biocrusts, tend to be a particular hotspot of complex bacterial and fungal interactions. Biocrust lichens can be colonized by other fungi or by other lichens, and they represent a particularly rich habitat for bacterial communities as shown by recent research results. Nevertheless, metabolic details and the regulatory principle of fungal and bacterial dynamics remain largely unclear and are in need of refined analysis. According to present data, biocrust bacteria and fungi seem to be widespread, diverse, and capable of withstanding the harsh and fluctuating conditions of biocrust habitats as long as stability of soil is warranted.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abed RM, Al-Sadi AM, AL-Shehi M, Al-Hinai S, Robinson MD (2013) Diversity of free-living and lichenized fungal communities in biological soil crusts of the Sultanate of Oman and their role in improving soil properties. Soil Biol Biochem 57:695–705

    Article  CAS  Google Scholar 

  • Abed RM, Al Kharusi S, 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 

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

    Article  CAS  PubMed  Google Scholar 

  • Angel R, Conrad R (2013) Elucidating the microbial resuscitation cascade in biological soil crusts following a simulated rain event. Environ Microbiol 15:2799–2815

    CAS  PubMed  Google Scholar 

  • Asta J, Orry F, Toutain F, Souchier B, Villemin G (2001) Micromorphological and ultrastructural investigations of the lichen-soil interface. Soil Biol Biochem 33:323–337

    Article  CAS  Google Scholar 

  • Bates ST, Garcia-Pichel F (2009) A culture independent study of free-living fungi in biological soil crusts of the Colorado Plateau: their diversity and relative contribution to microbial biomass. Environ Microbiol 11:56–67

    Article  CAS  PubMed  Google Scholar 

  • Bates ST, Reddy GSN, Garcia-Pichel F (2006) Exophiala crusticola anam. nov. (affinity Herpotrichiellaceae), a novel black yeast from biological soil crusts in the Western United States. Int J Syst Evol Microbiol 56:269–702

    Article  Google Scholar 

  • Bates ST, Garcia-Pichel F, Nash TH III (2010) Fungal components of biological soil crusts: insights from culture dependent and culture independent studies. Bibl Lichenol 105:197–210

    Google Scholar 

  • Bates ST, Nash TH III, Pichel F (2012) Patterns of diversity for fungal assemblages of biological soil crust from the southwestern United States. Mycologia 104:353–561

    Article  CAS  PubMed  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, vol 150. Springer, Berlin

    Google Scholar 

  • Bjelland T, Grube M, Hoem S, Jorgensen SL, Daae FL, Thorseth IH, Øvreås L (2010) Microbial metacommunities in the lichen–rock habitat. Environ Microbiol Rep 3:434–443

    Article  PubMed  Google Scholar 

  • Boyer SL, Johansen JR, Flechtner VR, Howard GL (2002) Phylogeny 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

    Article  CAS  Google Scholar 

  • Büdel B, Colesie C, Green ATG, 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 23(7):1639–1658, doi. 10.1007/s10531-014-0645-2

    Article  PubMed  PubMed Central  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 

  • Chan Y, Lacap DC, Lau MCY, Ha KY, Warren-Rhodes KA, Cockell CS, Cowan DA, McKay CP, Pointing SB (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14:2272–2282

    Article  PubMed  Google Scholar 

  • Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras-Alfaro A, Stursova M, Zeglin LH (2008) Pulse dynamics and microbial processes in aridland ecosystems. J Ecol 96:413–420

    Article  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 

  • da Rocha UN, Cadillo-Quiroz H, Karaoz U, Rajeev L, Klitgord N, Dunn S, Truong V, Buenrostro M, Bowen BP, Garcia-Pichel F, Mukhopadhyay A, Northen TR, Brodie EL (2015) Isolation of a significant fraction of non-phototroph diversity from a desert biological soil crust. Front Microbol 6:277

    Google Scholar 

  • Davies LO, Schäfer H, Marshall S, Bramke I, Oliver RG, Bending GD (2013) Light structures phototroph, bacterial and fungal communities at the soil surface. PloS One 8:e69048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de los Rios A, Grube M (2000) Host-parasite interfaces of some lichenicolous fungi in the Dacampiaceae (Dothideales, Ascomycota). Mycol Res 104:1348–1353

    Article  Google Scholar 

  • de los Rios A, Ascaso C, Grube M (2002) An ultrastructural, anatomical and molecular study of the lichenicolous lichen Rimularia insularis. Mycol Res 106:946–953

    Article  Google Scholar 

  • Delmont TO, Robe P, Cecillon S, Clark IM, Constancias F, Simonet P, Hirsch PR, Vogel TM (2011) Accessing the soil metagenome for studies of microbial diversity. Appl Environ Microbiol 77:1315–1324

    Article  CAS  PubMed  Google Scholar 

  • Elliott DR, Thomas AD, Hoon SR, Sen R (2014) Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari. Biodivers Conserv 23(7):1709–1733, doi. 10.1007/s10531-014-0684-8

    Article  Google Scholar 

  • Erlacher A, Cernava T, Cardinale M, Soh J, Sensen CW, Grube M, Berg G (2015) Rhizobiales as functional and endosymbiotic members in the lichen symbiosis of Lobaria pulmonaria L. Front Microbiol 6:53

    Article  PubMed  PubMed Central  Google Scholar 

  • Fierer N, Leff JW, Adams BJ, Nielsen UN, Bates ST, Lauber CL, Owens S, Gilbert JA, Wall DH, Caporaso GJ (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. PNAS 109:21390–21395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedl T (1987) Thallus development and phycobionts of the parasitic lichen Diploschistes muscorum. Lichenologist 19:183–191

    Article  Google Scholar 

  • Garcia-Pichel F, Wojciechowski MF (2009) The evolution of a capacity to build supra-cellular ropes enabled filamentous cyanobacteria to colonize highly erodible substrates. PLoS One 4:e7801

    Article  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • 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. Microb Ecol 46:312–321

    Article  CAS  PubMed  Google Scholar 

  • Gostincar C, Grube M, de Hoog S, Zalar P, Gunde-Cimerman N (2010) Extremotolerance in fungi: evolution on the edge. FEMS Microbiol Ecol 71:2–11

    Article  CAS  PubMed  Google Scholar 

  • Green LE, Porras-Alfaro A, Sinsabaugh RL (2008) Translocation of nitrogen and carbon integrates biotic crust and grass production in desert grassland. J Ecol 96:1076–1085

    Article  CAS  Google Scholar 

  • Grube M, Hafellner J (1990) Studien an flechtenbewohnenden Pilzen der Sammelgattung Didymella (Ascomycetes, Dothideales). Nova Hedwigia 51:283–360

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Grube M, Köberl M, Lackner S, Berg C, Berg G (2012) Host-parasite interaction and microbiome response: effects of fungal infections on the bacterial community of the Alpine lichen Solorina crocea. FEMS Microbiol Ecol 82:472–481

    Article  CAS  PubMed  Google Scholar 

  • Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, Wegner U, Becher D, Riedel K, Sensen CW, Berg G (2015) Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J 9:412–424

    Article  CAS  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. Microb Ecol 52:345–357

    Article  PubMed  Google Scholar 

  • Ives AR, Carpenter SR (2007) Stability and diversity of ecosystems. Science 317:58–62

    Article  CAS  PubMed  Google Scholar 

  • Johnson SL, Kuske CR, Carney TD, Housman DC, Gallegos-Graves L (2012) Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem. Glob Chang Biol 18:2583–2593

    Article  Google Scholar 

  • Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211

    Article  Google Scholar 

  • Kuske CR, Ticknor LO, Miller ME, Dunbar JM, Davis JA 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  PubMed Central  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  Google Scholar 

  • Lawrey JD, Diederich P (2011) Lichenicolous fungi—worldwide checklist, including isolated cultures and sequences. http://www.lichenicolous.net. Accessed 27 Jan 2012

  • Lombard N, Prestat E, van Elsas JD, Simonet P (2011) Soil-specific limitations for access and analysis of soil microbial communities by metagenomics. FEMS Microbiol Ecol 78:31–49

    Article  CAS  PubMed  Google Scholar 

  • Lumbsch HT, Ahti T, Altermann S, Paz ADG, Aptroot A, Arup U et al (2011) One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18:1–127

    Article  Google Scholar 

  • Maier S, Schmidt TSB, Zheng L, Peer T, Wagner V et al. (2014) Analyses of dryland biological soil crusts highlight lichens as an important regulator of microbial communities. Biodivers Conserv 23:1735–1755

    Article  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189

    Article  Google Scholar 

  • Marusenko Y, Huber DP, Hall SJ (2013) Fungi mediate nitrous oxide production but not ammonia oxidation in arid land soils of the southwestern US. Soil Biol Biochem 63:24–36

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Muggia L, Klug 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, 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  CAS  PubMed  Google Scholar 

  • Poelt J, Grube M (1993) Beiträge zur Kenntnis der Flechtenflora des Himalaya VIII. Lecanora subgen. Placodium. Nova Hedwigia 57:305–352

    Google Scholar 

  • Poelt J, Mayrhofer H (1988) Über Cyanotrophie bei Flechten. Plant Syst Evol 158:265–281

    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 

  • Ranzoni FV (1968) Fungi isolated in culture from soils of the Sonoran desert. Mycologia 60:356–371

    Article  CAS  PubMed  Google Scholar 

  • Reddy GSN, Garcia-Pichel F (2005) Dyadobacter crusticola sp. nov., from biological soil crusts in the Colorado Plateau, USA, and an emended description of the genus Dyadobacter Chelius and Triplett 2000. Int J Syst Evol Microbiol 55:1295–1299

    Article  CAS  PubMed  Google Scholar 

  • Reddy GSN, Garcia-Pichel F (2007) Sphingomonas mucosissima sp. nov. and Sphingomonas dessicabilis sp. nov., isolated from biological soil crusts in the Colorado Plateau, USA. Int J Syst Evol Microbiol 57:1028–1034

    Article  CAS  PubMed  Google Scholar 

  • Reddy GSN, Garcia-Pichel F (2009) Description of Patulibacter americanus sp. nov., isolated from biological soil crusts, emended description of the genus Patulibacter Takahashi et al. 2006 and proposal of Solirubrobacterales ord. nov. and Thermoleophilales ord. nov. Int J Syst Evol Microbiol 59:87–94

    Article  CAS  PubMed  Google Scholar 

  • Reddy GS, Garcia-Pichel F (2013) Description of Hymenobacter arizonensis sp. nov. from the southwestern arid lands of the United States of America. Antonie Van Leeuwenhoek 103:321–330

    Article  PubMed  Google Scholar 

  • Reddy GS, Garcia-Pichel F (2015) Description of Pseudomonas asuensis sp. nov. from biological soil crusts in the Colorado plateau, United States of America. J Microbiol 53:6–13

    Article  CAS  PubMed  Google Scholar 

  • Reddy GSN, Nagy M, Garcia-Pichel F (2006) Belnapia moabensis gen. nov., sp. nov., an alphaproteobacterium from biological soil crusts in the Colorado Plateau, USA. Int J Syst Evol Microbiol 56:51–58

    Article  CAS  PubMed  Google Scholar 

  • Reddy GSN, Potrafka R, Garcia-Pichel F (2007) Modestobacter versicolor sp. nov., an actinobacterium from biological soil crusts that produces melanins under oligotrophy, with emended descriptions of the genus Modestobacter and Modestobacter multiseptatus Mevs et al. 2000. Int J Syst Evol Microbiol 57:2014–2020

    Article  CAS  PubMed  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 10:1367–1374

    Article  Google Scholar 

  • Starkenburg SR, Reitenga KG, Freitas R, Johnson S, Chain RSG, Garcia-Pichel F, Kuske CR (2011) Genome of the cyanobacterium microcoleus vaginatus FGP-2, a photosynthetic ecosystem engineer of arid land soil biocrusts worldwide. J Bacteriol 193:4569–4570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • States JS (1978) Soil fungi of cool-desert plant communities in northern Arizona and South Utah. J Ariz Acad Sci 13:13–17

    Google Scholar 

  • States JS, Christensen M (2001) Fungi associated with biological soil crusts in desert grassland of Utah and Wyoming. Mycologia 93:432–439

    Article  Google Scholar 

  • Steven B, Gallegos-Graves l, Yeager CM, Belnap J, Evans RD et al (2012a) Dryland biological soil crust cyanobacteria show unexpected decreases in abundance under long-term elevated CO2. Environ Microbiol 14:3247–3258

    Article  CAS  PubMed  Google Scholar 

  • Steven B, Gallagos-Graves LV, Starkenburg SR, Chain PS, Kuske CR (2012b) Targeted and shotgun metagenomic approaches provide different descriptions of dryland soil microbial communities in a manipulated field study. Environ Microbiol Rep 4:248–256

    Article  PubMed  Google Scholar 

  • Steven B, Gallegos-Graves LV, Belnap J, Kuske CR (2013a) Dryland soil microbial communities display spatial biogeographic patterns associated with soil depth and soil parent material. FEMS Microbiol Ecol 86:101–113

    Article  CAS  PubMed  Google Scholar 

  • Steven B, Kuske C, Vincent WF (2013b) High bacterial diversity of biological soil crusts in water tracks over permafrost in the high arctic polar desert. Plos One 8(8):e71489, doi.10.1371/journal.pone.0071489

    Google Scholar 

  • Steven B, Gallegos-Graves L, Yeager C, Belnap J, Kuske CR (2014) Common and distinguishing features of the bacterial and fungal communities in biological soil crusts and shrub root zone soils. Soil Biol Biochem 69:302–312

    Article  CAS  Google Scholar 

  • Steven B, Hesse C, Gallegos-Graves LV, Belnap J, Kuske CR (2015) Fungal diversity in biological soil crusts of the Colorado plateau

    Google Scholar 

  • Wedin M, Maier S, Fernandez-Brime S, Cronholm B, Westberg M, Grube M (2015) Microbiome change by symbiotic invasion in lichens. Environ Microbiol, doi.10.1111/1462-2920.13032

  • 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeager CM, Kornosky JL, Morgan RE, Cain EC, Garcia-Pichel F, Housman DC et al. (2007) Three distinct clades of cultured heterocystous cyanobacteria constitute the dominant N2-fixing members of biological soil crusts of the Colorado Plateau, USA. FEMS Microbiol Ecol 60:85–97

    Article  CAS  PubMed  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 25:275–293

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Plant Sciences, University of Graz, Holteigasse 6, Graz, 8010, Austria

    Stefanie Maier & Martin Grube

  2. Department of Life Science, University of Trieste, Via Giorgieri 10, 34127, Trieste, Italy

    Lucia Muggia

  3. Bioscience Division, Los Alamos National Laboratory, Los Alamos, NM, 87545, USA

    Cheryl R. Kuske

Authors
  1. Stefanie Maier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lucia Muggia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cheryl R. Kuske
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martin Grube
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Grube .

Editor information

Editors and Affiliations

  1. Multiphase Chemistry Department, Max Plank Institute for Chemistry, Mainz, Germany

    Bettina Weber

  2. Plant Ecology and Systematics, Department of Biology, University of Kaiserslautern, Kaiserslautern, Germany

    Burkhard Büdel

  3. Southwest Biological Science Center, U.S. Geological Survey, Moab, Utah, USA

    Jayne Belnap

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Maier, S., Muggia, L., Kuske, C.R., Grube, M. (2016). Bacteria and Non-lichenized Fungi Within Biological Soil Crusts. In: Weber, B., Büdel, B., Belnap, J. (eds) Biological Soil Crusts: An Organizing Principle in Drylands. Ecological Studies, vol 226. Springer, Cham. https://doi.org/10.1007/978-3-319-30214-0_5

Download citation

Publish with us

Policies and ethics

Search

Navigation