Abstract
The Antarctic Dry Valleys are unable to support higher plant and animal life and so microbial communities dominate biotic ecosystem processes. Soil communities are well characterized, but rocky surfaces have also emerged as a significant microbial habitat. Here, we identify extensive colonization of weathered granite on a landscape scale by chasmoendolithic microbial communities. A transect across north-facing and south-facing slopes plus valley floor moraines revealed 30–100 % of available substrate was colonized up to an altitude of 800 m. Communities were assessed at a multidomain level and were clearly distinct from those in surrounding soils and other rock-inhabiting cryptoendolithic and hypolithic communities. All colonized rocks were dominated by the cyanobacterial genus Leptolyngbya (Oscillatoriales), with heterotrophic bacteria, archaea, algae, and fungi also identified. Striking patterns in community distribution were evident with regard to microclimate as determined by aspect. Notably, a shift in cyanobacterial assemblages from Chroococcidiopsis-like phylotypes (Pleurocapsales) on colder–drier slopes, to Synechococcus-like phylotypes (Chroococcales) on warmer–wetter slopes. Greater relative abundance of known desiccation-tolerant bacterial taxa occurred on colder–drier slopes. Archaeal phylotypes indicated halotolerant taxa and also taxa possibly derived from nearby volcanic sources. Among the eukaryotes, the lichen photobiont Trebouxia (Chlorophyta) was ubiquitous, but known lichen-forming fungi were not recovered. Instead, fungal assemblages were dominated by ascomycetous yeasts. We conclude that chasmoendoliths likely constitute a significant geobiological phenomenon at lower elevations in granite-dominated Antarctic Dry Valley systems.
Similar content being viewed by others
References
Thomas DSG (1997) Arid zones: Their nature and extent. In: Thomas DSG (ed) Arid zone geomorphology, 2nd edn. Wiley, Chichester, pp 3–12
Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562
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
Friedmann EI (1980) Endolithic microbial life in hot and cold deserts. Orig Life 10:223–235
Wierzchos J, de los Rios A, Ascaso C (2013) Microorganisms in desert rocks: the edge of life on earth. Int Microbiol 15:171–181
Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:68–74
Hugenholtz P, Goebel BM, Pace NR (1997) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774
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
Pointing SB et al (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci U S A 106:19964–19969
Sigler W, Bachofen R, Zeyer J (2003) Molecular characterization of endolithic cyanobacteria inhabiting exposed dolomite in central Switzerland. Environ Microbiol 5:618–627
Norris T, Castenholz R (2006) Endolithic photosynthetic communities within ancient and recent travertine deposits in Yellowstone National Park. FEMS Microbiol Ecol 57:470–483
Di Ruggiero J et al (2013) Microbial colonization of chasmoendolithic habitats in the hyper-arid zone of the Atacama Desert. Biogeosciences 10:2439–2450
Wong KY et al (2010) Hypolithic colonization of quartz pavement in the high altitude tundra of central Tibet. Microbial Ecol 60:730–739
Warren-Rhodes KA et al (2006) Hypolithic bacteria, dry limit of photosynthesis and microbial ecology in the hyperarid Atacama Desert. Microbial Ecol 52:389–398
Warren-Rhodes KA et al (2007) Lithic cyanobacterial ecology across environmental gradients and spatial scales in China’s hot and cold deserts. FEMS Microbiol Ecol 61:470–482
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
Chan Y et al (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14:2272–2282
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
Domínguez SG, Asencio AD (2011) Distribution of chasmoendolithic cyanobacteria in gypsiferous soils from semi-arid environments (SE Spain) by chemical and physical parameters. Nova Hedwig 92:1–27
Gerrath J, Matthes U, Larson D (2000) Endolithic algae and cyanobacteria from cliffs of the Niagara Escarpment, Ontario, Canada. Botany 78:807–815
De los Rios, Sancho LG, Grube M, Wierzchos J, Ascaso C (2005) Endolithic growth of two Lecidea lichens in granite from continental Antarctica detected by molecular and microscopy techniques. New Phytol 165:181–190
De los Ríos A, Grube M, Sancho LG, Ascaso C (2007) Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol 59:386–395
Lee CK et al (2012) The inter-valley soil comparative survey: the ecology of Dry Valley edaphic microbial communities. ISME J 6:1046–1057
Lee CK et al (2014) Complex drivers of biodiversity in a simple yet extreme terrestrial ecosystem. Ecol Lett
Wierzchos J, Ascaso C (1994) Application of back-scattered electron imaging to study the lichen–rock interface. J Microsc 175:54–59
Abdo Z et al (2006) Statistical method for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938
Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506
Cowell RK (2005) EstimateS: statistical estimation of species richness and shared species from samples. Version 7.7. http://www.purl.oclc.org/estimates
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Swofford DL (2002) PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Sunderland
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation, The University of Texas at Austin
Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143
Niederberger TD et al (2008) Microbial community composition in soils of Northern Victoria Land, Antarctica. Environ Microbiol 10:713–1724
Caruso T et al (2011) Stochastic and deterministic processes interact to determine global biogeography of arid soil bacteria. ISME J 5:1406–1413
Billi D et al (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492
Kuhl M et al (2005) A niche for bacteria containing chlorophyll d. Nature 433:820
Wong F et al (2010) Endolithic microbial colonization of limestone in a high-altitude arid environment. Microb Ecol 59:689–699
Friedmann EI, Kibler AP (1980) Nitrogen economy of endolithic microbial communities in hot and cold deserts. Microb Ecol 6:95–108
Billi D, Potts M (2002) Life and death of dried prokaryotes. Res Microbiol 153:7–12
Cox MM, Battista JR (2005) Deinococcus radiodurans — the consummate survivor. Nat Rev Microbiol 3:882–892
Rajeev L et al (2013) Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust. ISME J 7:2178–2191
Chan Y et al (2013) Functional ecology of an Antarctic Dry Valley. Proc Natl Acad Sci U S A 110:8990–8995
Bottos E et al (2014) Airborne bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica. Microb Ecol 67:120–128
Friedl T, Büdel B (2008) Photobionts. In: Nash TH III (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 7–26
Ahmadjian V (1988) The lichen alga Trebouxia: does it occur free-living? Plant Syst Evol 158:243–247
Bubrick P, Galun M, Frensdorff A (1984) Observations on free-living Trebouxia DePuymaly and Pseudotrebouxia Archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th. Fr. can be found free-living in nature. New Phytol 97:455–462
Mukhtar A, Garty J, Galun M (1994) Does the lichen alga Trebouxia occur free-living in nature: further immunological evidence. Symbiosis 17:247–253
Rao S et al (2011) Low-diversity fungal assemblage in an Antarctic Dry Valleys soil. Polar Biol 35:567–574
Hirsch P, Eckhardt FEW, Palmer RJ Jr (1995) Fungi active in weathering of rock and stone monuments. Can J Bot 73:1384–1390
Convey P, Stevens MI (2007) Antarctic biodiversity. Science 317:1877–1878
Cockell CS, Stokes DM (2004) Widespread colonization by polar hypoliths. Nature 431:414
Cowan DA et al (2011) Distribution and abiotic influences on hypolithic microbial communities in an Antarctic Dry Valley. Polar Biol 34:307–311
Cowan DA et al (2011) Hypolithic communities: important nitrogen sources in Antarctic soils. Environ Microbiol Rep 3:581–586
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
Bahl J et al (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:163. doi:10.1038/ncomms1167
Viles H (1995) Ecological perspectives on rock surface weathering: towards a conceptual model. Geomorphology 13:21–35
De los Ríos A, Wierzchos J, Sancho LG, Ascaso C (2003) Acid microenvironmens in microbial biofilms of Antarctica endolithic mycroecosystems. Environ Microbiol 5:231–237
Buedel B et al (2004) Reshaping of sandstone surfaces by cryptoendolithic cyanbacteria: bioalkination causes chemical weathering in arid landscapes. Geobiology 2:261–268
Acknowledgments
The authors are extremely grateful to Antarctica New Zealand for logistics and field support in Antarctica. This research was supported by Foundation for Research, Science and Technology of New Zealand (UOWX0710 and UOWX0715). A.delR, SPO were supported by grant CTM2012-3822-C02-02 from the Spanish Ministry of Economy and Competition. CKL and SCC were supported by the New Zealand Marsden Fund (UOW1003 and UOW0802).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 1641 kb)
Rights and permissions
About this article
Cite this article
Yung, C.C.M., Chan, Y., Lacap, D.C. et al. Characterization of Chasmoendolithic Community in Miers Valley, McMurdo Dry Valleys, Antarctica. Microb Ecol 68, 351–359 (2014). https://doi.org/10.1007/s00248-014-0412-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-014-0412-7