Skip to main content

Advertisement

SpringerLink
Log in

Species-specific nitrogenase activity in lichen-dominated biological soil crusts from the Colorado Plateau, USA

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aim

Biological soil crusts (biocrusts) play numerous crucial roles in drylands, which comprise over 40% of Earth’s terrestrial surface. Among these key contributions is the fixation of atmospheric nitrogen. Yet, relatively little is known about the N2 fixation capabilities of different lichen species that are found in late successional biocrust communities across drylands globally.

Methods

In order to improve our species-specific understanding of biocrust lichen N2 fixation, we collected biocrusts dominated by four common species of lichens – Collema spp., Gyalolechia desertorum, Psora decipiens, and Squamarina lentigera – that represent a range of lichen families and morphological types. Nitrogenase activity of the biocrust community dominated by these lichens was evaluated using the acetylene reduction assay. Additionally, biocrust community composition was assessed using the point-intercept method along transects at varied distances from exposed bedrock.

Results

As expected, Collema spp.-dominated biocrusts had the highest rates of nitrogenase activity, with rates up to seven times larger than those of the other three target species. Nitrogen concentrations and carbon:nitrogen ratios of lichen tissue differed among lichen species. However, when the composite biocrust profile was assessed (i.e., biocrust tissue, microbial cells, and mineral soil to a 2 cm depth) these among-species differences in total nitrogen disappeared. Community composition changed according to distance from exposed bedrock, with a higher diversity of lichens closer to the bedrock.

Conclusion

Multiple drivers, including climate and land use change, affect biocrust community composition and species-specific functional information, even within a group such as late successional biocrusts, could help in forecasting the potential effects of global change on N2 fixation, and consequently, soil fertility in drylands.

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

Similar content being viewed by others

References

  • Antoninka A, Bowker MA, Reed SC, Doherty K (2016) Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor Ecol 24:324–335

    Article  Google Scholar 

  • Antoninka A, Bowker MA, Chuckran P, Barger NN, Reed S, Belnap J (2017) Maximizing establishment and survivorship of field-collected and greenhouse-cultivated biocrusts in a semi-cold desert. Plant Soil 413:1–13

    Article  CAS  Google Scholar 

  • Aschenbrenner IA, Cernava T, Berg G, Grube M (2016) Understanding microbial multi-species symbioses. Front Microbiol 7:180

    Article  PubMed  PubMed Central  Google Scholar 

  • Barger NN, Castle SC, Dean GN (2013) Denitrification from nitrogen-fixing biologically crusted soils in a cool desert environment, southeast Utah, USA. Ecol Process 2:16

    Article  Google Scholar 

  • Barger NN, Weber B, Garcia-Pichel F, Zaady E, Belnap J (2016) Patterns and controls on nitrogen cycling of biological soil crusts. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands, ecological studies volume 226. Springer, Switzerland, pp 257–285

    Chapter  Google Scholar 

  • Belnap J (1996) Soil surface disturbances in cold deserts: effects on nitrogenase activity in cyanobacterial-lichen soil crusts. Biol Fertil Soils 23:362–367

    Article  CAS  Google Scholar 

  • Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–135

    Article  CAS  Google Scholar 

  • Belnap J, Lange OL (2003) Biological soil crusts: structure, function, and management. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Belnap J, Phillips SL, Witwicki DL, Miller ME (2008) Visually assessing the level of development and soil surface stability of cyanobacterially dominated biological soil crusts. J Arid Environ 72:1257–1264

    Article  Google Scholar 

  • Belnap J, Weber B, Büdel B (2016) Biological soil crusts as an organizing principle in drylands. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands, ecological studies volume 226. Springer, Switzerland, pp 3–13

    Chapter  Google Scholar 

  • Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23

    Article  Google Scholar 

  • Bowker MA, Maestre FT, Eldridge D, Belnap J, Castillo-Monroy A, Escolar C, Soliveres S (2014) Biological soil crusts (biocrusts) as a model system in community, landscape and ecosystem ecology. Biodivers Conserv 23:1619–1637

    Article  Google Scholar 

  • Bowker MA, Belnap J, Büdel B, Sannier C, Pietrasiak N, Eldridge DJ, Rivera-Aguilar V (2016) Controls on distribution patterns of biological soil crusts at micro-to global scales. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands, ecological studies volume 226. Springer, Switzerland, pp 173–197

    Chapter  Google Scholar 

  • Castillo-Monroy AP, Bowker MA, Maestre FT, Rodríguez-Echeverría S, Martinez I, Barraza-Zepeda CE, Escolar C (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 

  • Elbert W, Weber B, Burrows S, Steinkamp J, Büdel B, Andreae MO, Pöschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462

    Article  CAS  Google Scholar 

  • Escolar C, Martínez I, Bowker MA, Maestre FT (2012) Warming reduces the growth and diversity of biological soil crusts in a semi-arid environment: implications for ecosystem structure and functioning. Philos Trans R Soc Lond Ser B Biol Sci 367:3087–3099

    Article  Google Scholar 

  • Ferrenberg S, Reed SC, Belnap J (2015) Climate change and physical disturbance cause similar community shifts in biological soil crusts. PNAS 112:12116–12121

    Article  PubMed  CAS  Google Scholar 

  • Ferrenberg S, Tucker CL, Reed SC (2017) Biological soil crusts: diminutive communities of potential global importance. Front Ecol Environ 15:160–167

    Article  Google Scholar 

  • Grube M, Berg G (2009) Microbial consortia of bacteria and fungi with focus on the lichen symbiosis. Fungal Biol Rev 23:72–85

    Article  Google Scholar 

  • Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-reduction assay for N2 fixation: laboratory and field evaluation. Plant Physiol 43:1185–1207

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hartley A, Barger N, Belnap J, Okin GS (2007) Dryland ecosystems. In: Marschner P, Rengel Z (eds) Nutrient cycling in terrestrial ecosystems. Soil Biology, vol 10. Springer, Berlin

  • Honegger R (2001) The symbiotic phenotype of lichen-forming ascomycetes. In: Hock B (ed) The Mycota IX. Springer-Verlag, Berling, pp 165–188

    Google Scholar 

  • Honegger R (2008) Morphogenesis. In: Nash THIII (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 69–93

    Chapter  Google Scholar 

  • Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293

    CAS  Google Scholar 

  • Housman DC, Powers HH, Collins AD, Belnap J (2006) Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert. J Arid Environ 66:620–634

    Article  Google Scholar 

  • Johnson SL, Neuer S, Garcia-Pichel F (2007) Export of nitrogenous compounds due to incomplete cycling withing biological soil crusts of arid lands. Environ Microbiol 9:680–689

    Article  PubMed  CAS  Google Scholar 

  • Jonasson S (1983) The point intercept method for non-destructive estimation of biomass. Phytocoenologia 11:385–388

    Article  Google Scholar 

  • Kershaw KA (1985) Physiological ecology of lichens. Cambridge University Press, Cambridge

    Google Scholar 

  • Ley RE, D’Antonio CM (1998) Exotic grass invasion alters potential rates of N fixation in Hawaiian woodlands. Oecologia 113:179–187

    Article  PubMed  Google Scholar 

  • Liu YR, Delgado-Baquerizo M, Trivedi P, He JZ, Singh BK (2016) Species identify of biocrust-forming lichens drives the response of soil nitrogen cycle to altered precipitation frequency and nitrogen amendment. Soil Biol Biochem 96:128–136

    Article  CAS  Google Scholar 

  • McKay CP (2016) Water sources for cyanobacteria below desert rocks in the Negev Desert determined by conductivity. Glob Ecol Conserv 6:145–151

    Article  Google Scholar 

  • Maestre FT, Castillo-Monroy AP, Bowker MA, Ochoa-Hueso R (2012a) Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. J Ecol 100:317–330

    Article  CAS  Google Scholar 

  • Maestre FT, Salguero-Gómez R, Quero JL (2012b) It is getting hotter in here: determining and projecting the impacts of global environmental change on drylands. Philos Trans R Soc Lond Ser B Biol Sci 367:3062–3075

    Article  Google Scholar 

  • Marsh J, Nouvet S, Sanborn P, Coxson D (2006) Composition and function of biological soil crust communities along topographic gradients in grasslands of central interior British Columbia (Chilcotin) and southwestern Yukon (Kluane). Can J Bot 84:717–736

    Article  Google Scholar 

  • McHugh TA, Morrissey EM, Mueller RC, Gallegos-Graves LV, Kuske CR, Reed SC (2017) Bacterial, fungal, and plant communities exhibit no biomass or compositional response to two years of simulated nitrogen deposition in a semiarid grassland. Environ Microbiol 19:1600–1611

    Article  PubMed  CAS  Google Scholar 

  • Nash THIII (1996) Lichen biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Palmqvist K, Campbell D, Ekblad A, Johansson H (1998) Photosynthetic capacity in relation to nitrogen content and its partitioning in lichens with different photobionts. Plant Cell Environ 21:361–372

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Porras-Alfaro A, Ndinga C, Hamm PS, Torres-Cruz TJ, Kuske CR (2017) Fungal diversity, community structure and their functional roles in desert soils. In: Steven B (ed) The biology of arid soils, life in extreme environments, volume 4. De Gruyter, pp 97–122

  • Rai A, Bergman B (2002) Cyanolichens. (Spl. Issue-biology and environment). Proc Royal Irish Acad 102:19–22

    Article  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol S 42:489–512

    Article  Google Scholar 

  • Reed SC, Coe KK, Sparks JP, Housman DC, Zelikova TJ, Belnap J (2012) Changes to dryland rainfall result in rapid moss mortality and altered soil fertility. Nat Clim Chang 2:752–755

    Article  CAS  Google Scholar 

  • Reed SC, Maestre FT, Ochoa-Hueso R, Kuske CR, Darrouzet-Nardi A, Oliver M, Darby B, Sancho LG, Sinsabaugh RL, Belnap J (2016) Structure, composition, and function of biocrust lichen communities. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands, ecological studies volume 226. Springer, Switzerland, pp 451–476

    Chapter  Google Scholar 

  • Rikkinen J (2007) Relations between cyanobacterial symbionts in lichens and plants. In: Pawlowski K (ed) Prokaryotic symbionts in plants. Microbiology monographs, vol 8. Springer, Berlin

    Google Scholar 

  • Rosentreter R, Bowker M, Belnap J (2007) A field guide to biological soil crusts of western U.S. drylands. U.S. Government Printing Office, Denver

    Google Scholar 

  • Rosentreter R, Eldridge DJ, Westberg M, Williams L, Grube M (2016) Structure, composition, and function of biocrust lichen communities. In: Weber B, Büdel B, Belnap J (eds) Biological soil crusts: an organizing principle in drylands, ecological studies volume 226. Springer, Switzerland, pp 121–157

    Chapter  Google Scholar 

  • Russow R, Veste M, Böhme F (2005) A natural 15N approach to determine the biological fixation of atmospheric nitrogen by biological soil crusts of the Negev Desert. Rapid Commun Mass Spectrom 19:3451–3456

    Article  PubMed  CAS  Google Scholar 

  • Steven B, 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 

  • Wierzchos J, de los Rios A, Ascaso C (2012) Microorganisms in desert rocks: the edge of life on earth. Int Microbiol 15:171–181

    Google Scholar 

Download references

Acknowledgements

The authors thank Matthew Bowker and Anita Antoninka for their assistance with lichen identification, and Hilda Smith for help with gas chromatography. We are also grateful to Natalie Day, David Eldridge, and three anonymous reviewers, whose comments on an earlier draft significantly improved the paper. This research was supported by the U.S. Department of Energy Office of Science Terrestrial Ecosystem Sciences Program, under Award Number DE-SC-0008168, as well as the US Geological Survey’s Ecosystems Mission Area. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Authors and Affiliations

  1. US Geological Survey, Southwest Biological Science Center, 2290 SW Resource Blvd, Moab, UT, 84532, USA

    Terry J. Torres-Cruz, Armin J. Howell, Robin H. Reibold & Sasha C. Reed

  2. Department of Biological Sciences, Colorado Mesa University, 1100 North Ave, Grand Junction, CO, 81501, USA

    Theresa A. McHugh & Mackenzie A. Eickhoff

Authors
  1. Terry J. Torres-Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Armin J. Howell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robin H. Reibold
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Theresa A. McHugh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mackenzie A. Eickhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sasha C. Reed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sasha C. Reed.

Additional information

Responsible Editor: David John Eldridge

Electronic supplementary material

ESM 1

(PDF 429 kb)

ESM 2

(PDF 163 kb)

ESM 3

(PDF 67.1 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Torres-Cruz, T.J., Howell, A.J., Reibold, R.H. et al. Species-specific nitrogenase activity in lichen-dominated biological soil crusts from the Colorado Plateau, USA. Plant Soil 429, 113–125 (2018). https://doi.org/10.1007/s11104-018-3580-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3580-2

Keywords

Search

Navigation