Skip to main content
SpringerLink
Log in

Diverse metabolic and stress-tolerance pathways in chasmoendolithic and soil communities of Miers Valley, McMurdo Dry Valleys, Antarctica

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The majority of biomass in the McMurdo Dry Valleys of Antarctica occurs within rocks and soils, but despite the wealth of biodiversity data very little is known about the potential functionality of communities within these substrates. The putative physiological capacity of microbial communities in granite boulders (chasmoendoliths) and soils of a maritime-influenced Antarctic Dry Valleys were interrogated using the GeoChip microarray. Diversity estimates revealed surprisingly high diversity and evenness in both communities, with Chlorobi and Deinococci in soils accounting for major differences between the substrates. Autotrophs were more diverse in chasmoendoliths, and diazotrophs more diverse in soils. Both substrates revealed a previously unappreciated abundance of Halobacteria (Archaea), Ascomycota (Fungi) and Basidiomycoyta (Fungi). The fungi accounted for much of the differences between substrates in metabolic pathways associated with carbon transformations, particularly for aromatic compounds. Nitrogen fixation genes were more common in soils, although nitrogen catabolism genes were abundant in chasmoendoliths. Stress response pathways were more diverse in chasmoendoliths, possibly reflecting greater environmental stress in this exposed substrate compared with subsurface soils. Overall diversity of stress-tolerance genes was markedly lower than that recorded for inland locations where environmental stress is exacerbated. We postulate that the chasmoendolithic community occupies a key role in biogeochemical transformations in Dry Valley systems where granite substrates are abundant among open soils. The findings indicate that a substantial upward revision to estimates of biologically active surfaces in this system is warranted.

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

  • Arenz BE et al (2006) Fungal diversity in soils and historic wood from the Ross Sea region of Antarctica. Soil Biol Biochem 38:3057–3064

    Article  CAS  Google Scholar 

  • Bahl J et al (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:163. doi:10.1038/ncomms1167

    Article  PubMed Central  PubMed  Google Scholar 

  • Bottos E et al (2013) Airborne bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica. Microb Ecol 67:120–128

    Article  PubMed Central  Google Scholar 

  • Caruso T et al (2011) Stochastic and deterministic processes interact to determine global biogeography of arid soil bacteria. ISME J 5:1406–1413

    Article  PubMed Central  PubMed  Google Scholar 

  • Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8:129–138

    Article  CAS  PubMed  Google Scholar 

  • Chan Y et al (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14:2272–2282

    Article  PubMed  Google Scholar 

  • Chan Y et al (2013) Functional ecology of an Antarctic dry valley. Proc Natl Acad Sci USA 110:8990–8995

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Cowan DA et al (2011) Distribution and abiotic influences on hypolithic microbial communities in an Antarctic dry valley. Polar Biol 34:307–311

    Article  Google Scholar 

  • de La Torre J, Goebel B, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69:3858–3867

    Article  PubMed Central  PubMed  Google Scholar 

  • de los Rios A, Wierzchos J, Sancho LG, Ascaso C (2004) Exploring the physiological state of continental Antarctic endolithic microorganisms by microscopy. FEMS Microbiol Ecol 50:143–152

    Article  Google Scholar 

  • de los Rios A et al (2005) Endolithic growth of two Lecidea lichens in granite from continental Antarctica detected by molecular and microscopy techniques. New Phytol 165:181–190

    Article  PubMed  Google Scholar 

  • de los Ríos A, Wierzchos J, Sancho LG, Ascaso C (2007) Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol 59:386–395

    Article  Google Scholar 

  • Doran PT et al (2002) Valley floor climate observations from the McMurdo Dry Valleys, Antarctica, 1986–2000. J Geophys Res 107(D24):4772. doi:10.1029/2001JD002045

    Article  Google Scholar 

  • Elbert W et al (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462

    Article  CAS  Google Scholar 

  • Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fraser CI et al (2014) Geothermal activity helps life survive glacial cycles. Proc Natl Acad Sci USA 111:5634–5639

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:68–74

    Article  Google Scholar 

  • Friedmann EI, Kibler AP (1980) Nitrogen economy of endolithic microbial communities in hot and cold deserts. Microb Ecol 6:95–108

    Article  CAS  PubMed  Google Scholar 

  • Friedmann EI, Kappen L, Meyer MA, Neinow JA (1993) Long-term productivity in the cryptoendolithic community of the Ross Desert, Antarctica. Microb Ecol 25:51–69

    Article  CAS  PubMed  Google Scholar 

  • He Z et al (2007) GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME J 1:67–77

    Article  CAS  PubMed  Google Scholar 

  • Lee CK et al (2012) The inter-valley soil comparative survey: the ecology of Dry Valley edaphic microbial communities. ISME J 6:1046–1057

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maghales C et al (2012) At limits of life: multidisciplinary insights reveal environmental constraints on biotic diversity in continental Antarctica. PLoS One. doi:10.1371/journal.pone.0044578

    Google Scholar 

  • Ng KW, Pointing SB, Dvornyk V (2013) Patterns of nucleotide diversity in the idpA circadian gene in closely related species of cyanobacteria from extreme cold deserts. Appl Environ Microbiol 79:1516–1522

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Niederberger TD et al (2012) Diverse and highly active diazotrophic assemblages inhabit ephemerally wetted soils of the Antarctic Dry Valleys. FEMS Microbiol Ecol 82:376–390

    Article  CAS  PubMed  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 

  • Pointing SB et al (2007) Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China’s hot and cold hyperarid deserts. Environ Microbiol 9:414–424

    Article  CAS  PubMed  Google Scholar 

  • Pointing SB et al (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA 106:19964–19969

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pointing SB, Bollard-Breen B, Gillman LN (2014) Diverse cryptic refuges for life during glaciation. Proc Natl Acad Sci USA 111:5452–5453

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rao S et al (2011) Low-diversity fungal assemblage in an Antarctic Dry Valleys soil. Polar Biol 35:567–574

    Article  Google Scholar 

  • Scientific Committee on Antarctic Research (2004) SCAR Bulletin #155. Polar Rec 40:371–382

    Article  Google Scholar 

  • Thomas DSG (1997) Arid zones: their nature and extent. In: Thomas DSG (ed) Arid zone geomorphology, 2nd edn. Wiley, Chichester, pp 3–12

    Google Scholar 

  • Wierzchos J, de los Rios A, Ascaso C (2013) Microorganisms in desert rocks: the edge of life on Earth. Int Microbiol 15:171–181

    Google Scholar 

  • Wong KY et al (2010a) Hypolithic colonization of quartz pavement in the high altitude tundra of central Tibet. Microb Ecol 60:730–739

    Article  PubMed Central  PubMed  Google Scholar 

  • Wong KY et al (2010b) Endolithic microbial colonization of limestone in a high-altitude arid environment. Microb Ecol 59:689–699

    Article  PubMed  Google Scholar 

  • Wynn-Williams DD (1990) Ecological aspects of Antarctic microbiology. Adv Microb Ecol 11:71–146

    Article  Google Scholar 

  • Yung C et al (2014) Characterization of chasmoendolithic community in Miers Valley, McMurdo Dry Valleys, Antarctica. Microb Ecol 68:351–359

    PubMed  Google Scholar 

  • Zhou J et al (2008) Spatial scaling of functional gene diversity across various microbial taxa. Proc Natl Acad Sci USA 105:7768–7773

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the Institute for Applied Ecology New Zealand. The development of the GeoChip and associated computational pipelines used in this study was supported by Ecosystems and Networks Integrated with Genes and Molecular Assemblies (ENIGMA) through the US Department of Energy (DE-AC02-05CH11231). J. Zhou and J. D. Van Nostrand’s efforts were supported by the US Department of Energy (DE-SC0004601) and the US National Science Foundation (EF-1065844). The authors are extremely grateful to Antarctica New Zealand for logistics and field support in Antarctica.

Author information

Authors and Affiliations

  1. Institute for Applied Ecology New Zealand, School of Applied Sciences, Auckland University of Technology, Private Bag 92006, Auckland, 1142, New Zealand

    Sean T. S. Wei, Yuki Chan, Annapoorna Maitrayee Ganeshram & Stephen B. Pointing

  2. Centro de Ciencias Medioambientales, C/Serrano 115 Duplicado, 28006, Madrid, Spain

    Miguel-Angel Fernandez-Martinez & Asuncion de los Rios-Murillo

  3. Department of Microbiology and Plant Biology, Institute for Environmental Genomics, University of Oklahoma, Norman, OK, 73019, USA

    Joy D. Van Nostrand & Jizhong Zhou

  4. Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China

    Jill M. Y. Chiu

  5. International Centre for Terrestrial Antarctic Research, University of Waikato, Private Bag 3105, Hamilton, 3240, New Zealand

    S. Craig Cary & Stephen B. Pointing

  6. Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

    Jizhong Zhou

  7. State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing, 100084, China

    Jizhong Zhou

Authors
  1. Sean T. S. Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miguel-Angel Fernandez-Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yuki Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joy D. Van Nostrand
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Asuncion de los Rios-Murillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jill M. Y. Chiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Annapoorna Maitrayee Ganeshram
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Craig Cary
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jizhong Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Stephen B. Pointing
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen B. Pointing.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, S.T.S., Fernandez-Martinez, MA., Chan, Y. et al. Diverse metabolic and stress-tolerance pathways in chasmoendolithic and soil communities of Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biol 38, 433–443 (2015). https://doi.org/10.1007/s00300-014-1598-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-014-1598-3

Keywords

Search

Navigation