Advertisement

Polar Biology

, Volume 40, Issue 5, pp 997–1006 | Cite as

Endolithic microbial diversity in sandstone and granite from the McMurdo Dry Valleys, Antarctica

  • Stephen D. J. Archer
  • Asuncion de los Ríos
  • Kevin C. Lee
  • Thomas S. Niederberger
  • S. Craig Cary
  • Kathryn J. Coyne
  • Susanne Douglas
  • Donnabella C. Lacap-Bugler
  • Stephen B. PointingEmail author
Original Paper

Abstract

Cryptic microbial communities develop within rocky substrates in Antarctica’s McMurdo Dry Valleys as a stress avoidance strategy. They may be cryptoendolithic within pore spaces of weathered rocks, or develop in cracks and fissures as chasmoendolithic communities and are characterised by coloured bands of colonisation. Here we used a precision drill to recover fractions from black, white, green and red layers within colonised granite and sandstone. We combined backscattered scanning electron microscopy and high-throughput sequencing to identify major taxa in each band. We confirmed the presence of algal and fungal lichen symbionts, cyanobacteria and free-living algae, plus a diverse heterotrophic bacterial and archaeal component. A clear delineation at the community level was observed. The relatively biodiverse and heterogenous lichen communities occurred in weathered sandstone cliffs, whilst in granite and sandstone boulders, cyanobacterial communities were dominant. Differences between coloured bands of colonisation within each community were less clear. The study demonstrates that endolithic microbial communities can be recovered using a drill technology similar to that planned for the search for endolithic biosignatures on Mars.

Keywords

Antarctica Astrobiology Chasmoendolith Cryptoendolith Cyanobacteria Lichen 

Notes

Acknowledgments

The authors wish to acknowledge Antarctica New Zealand for logistics and field support in Antarctica. Research was supported financially by NASA (EPSCoR-RID fund), the Institute for Applied Ecology New Zealand (www.aenz.aut.ac.nz) and Grants to Dr de los Ríos (CTM2012-38222-C02-02 from the MINECO and PRX15/00478 Salvador Madariaga from the MEC, Spain).

Supplementary material

300_2016_2024_MOESM1_ESM.pdf (127 kb)
Supplementary material 1 (PDF 127 kb)

References

  1. Aislabie JM, Chhour KL, Saul DJ et al (2006) Dominant bacteria in soils of Marble Point and Wright Valley, Victoria Land, Antarctica. Soil Biol Biochem 38:3041–3056. doi: 10.1016/j.soilbio.2006.02.018 CrossRefGoogle Scholar
  2. Bahl J, Lau MCY, Smith GJD et al (2011) Ancient origins determine global biogeography of hot and cold desert cyanobacteria. Nat Commun 2:163. doi: 10.1038/ncomms1167 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Broady PA (1981) The ecology of chasmolithic algae in coastal locations in Antarctica. Phycologia 20:259–272. doi: 10.2216/i0031-8884-20-3-259.1 CrossRefGoogle Scholar
  4. Cámara B, Suzuki S, Nealson KH et al (2014) Ignimbrite textural properties as determinants of endolithic colonization patterns from hyper-arid Atacama Desert. Int Microbiol 17:235–247. doi: 10.2436/20.1501.01.226 PubMedGoogle Scholar
  5. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi: 10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Caruso T, Chan Y, Lacap DC et al (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5:1406–1413. doi: 10.1038/ismej.2011.21 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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. doi: 10.1038/nrmicro2281 CrossRefPubMedGoogle Scholar
  8. Chan Y, Lacap DC, Lau MCY et al (2012) Hypolithic microbial communities: between a rock and a hard place. Environ Microbiol 14:2272–2282. doi: 10.1111/j.1462-2920.2012.02821.x CrossRefPubMedGoogle Scholar
  9. Chan Y, Van Nostrand JD, Zhou J et al (2013) Functional ecology of an Antarctic Dry Valley. Proc Natl Acad Sci USA 110:8990–8995. doi: 10.1073/pnas.1300643110 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Darienko T, Gustavs L et al (2015) Evaluating the species boundaries of green microalgae (Coccomyxa, Trebouxiophyceae, Chlorophyta) using integrative taxonomy and DNA barcoding with further implications for the species identification in environmental samples. PloS one 10(6):e0127838. doi: 10.1371/journal.pone.0127838 CrossRefPubMedPubMedCentralGoogle Scholar
  11. de La Torre JR, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Env Microbiol 69:3858–3867. doi: 10.1128/AEM.69.7.3858-3867.2003 CrossRefGoogle Scholar
  12. de los Ríos A, Grube M, Sancho LG et al (2007) Ultrastructural and genetic characteristics of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol 59:386–395. doi: 10.1111/j.1574-6941.2006.00256.x CrossRefPubMedGoogle Scholar
  13. de los Ríos A, Cary C, Cowan D (2014a) The spatial structures of hypolithic communities in the Dry Valleys of East Antarctica. Polar Biol 37:1823–1833. doi: 10.1007/s00300-014-1564-0 CrossRefGoogle Scholar
  14. de los Ríos 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. doi: 10.1016/j.femsec.2004.06.010 CrossRefPubMedGoogle Scholar
  15. de los Ríos A, Wierzchos J, Sancho LG et al (2005) Ecology of endolithic lichens colonizing granite in continental Antarctica. Lichenol 37:383. doi: 10.1017/S0024282905014969 CrossRefGoogle Scholar
  16. de los Ríos A, Wierzchos J, Ascaso C (2014b) The lithic microbial ecosystems of Antarctica’s McMurdo Dry Valleys. Antarct Sci 26:459–477. doi: 10.1017/S0954102014000194 CrossRefGoogle Scholar
  17. Friedmann EI (1980) Endolithic microbial life in hot and cold deserts. Orig Life 10:223–235CrossRefPubMedGoogle Scholar
  18. Friedmann EI (1982) Endolithic microorganisms in the antarctic cold desert. Science 215:1045–1053. doi: 10.1126/science.215.4536.1045 CrossRefPubMedGoogle Scholar
  19. Friedmann EI, Ocampo R (1976) Endolithic blue-green algae in the dry valleys: primary producers in the antarctic desert ecosystem. Science 193:1247–1249. doi: 10.1126/science.193.4259.1247 CrossRefPubMedGoogle Scholar
  20. Friedmann E, Hua M, Ocampo-Friedmann R (1988) Cryptoendolithic lichen and cyanobacteria communities of the Ross Desert, Antarctica. Polarforschung 58:251–259PubMedGoogle Scholar
  21. Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Micro 9:791–802. doi: 10.1038/nrmicro2649 CrossRefGoogle Scholar
  22. Gomez-Alvarez V, King GM et al (2007) Comparative bacterial diversity in recent Hawaiian volcanic deposits of different ages. FEMS Microbiol Ecol 60(1):60–73. doi: 10.1111/j.1574-6941.2006.00253.x CrossRefPubMedGoogle Scholar
  23. Lee CK, Barbier BA, Bottos EM et al (2012) The Inter-Valley Soil Comparative Survey: the ecology of Dry Valley edaphic microbial communities. ISME J 6:1046–1057. doi: 10.1038/ismej.2011.170 CrossRefPubMedGoogle Scholar
  24. Marnocha CL, Dixon JC (2014) Endolithic bacterial communities in rock coatings from Karkevagge, Swedish Lapland. FEMS Microbiol Ecol 90(2):533–542. doi: 10.1111/1574-6941.12415 PubMedGoogle Scholar
  25. Moorhead DL, Doran PT, Fountain AG et al (1999) Ecological Legacies: impacts on Ecosystems of the McMurdo Dry Valleys. Bioscience 49:1009–1019. doi: 10.1525/bisi.1999.49.12.1009 CrossRefGoogle Scholar
  26. Nicolaus B, Panico A, Lama L et al (1999) Chemical composition and production of exopolysaccharides from representative members of heterocystous and non-heterocystous cyanobacteria. Phytochemistry 52:639–647. doi: 10.1016/S0031-9422(99)00202-2 CrossRefGoogle Scholar
  27. Niederberger TD, McDonald IR, Hacker AL et al (2008) Microbial community composition in soils of Northern Victoria Land, Antarctica. Env Microbiol 10:1713–1724. doi: 10.1111/j.1462-2920.2008.01593.x CrossRefGoogle Scholar
  28. Niederberger TD, Sohm JA, Tirindelli J et al (2012) Diverse and highly active diazotrophic assemblages inhabit ephemerally wetted soils of the Antarctic Dry Valleys. FEMS Microbiol Ecol 82:376–390. doi: 10.1111/j.1574-6941.2012.01390.x CrossRefPubMedGoogle Scholar
  29. Pointing S (2016) Hypolithic communities. In: Weber B, Budel B, Belnap J (eds) Biological soil crusts: an organising principle in drylands, Ecological Studies Series 226, Springer, Berlin, pp 199–2933. doi: 10.1007/978-3-319-30214-0
  30. Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Micro 10:551–562. doi: 10.1038/nrmicro2831 CrossRefGoogle Scholar
  31. Pointing SB, Chan Y, Lacap DC et al (2009) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA 106:19964–19969. doi: 10.1073/pnas.0908274106 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Pointing SB, Bollard-Breen B, Gillman LN (2014) Diverse cryptic refuges for life during glaciation. Proc Natl Acad Sci USA. doi: 10.1073/pnas.1403594111 PubMedPubMedCentralGoogle Scholar
  33. Pointing S, Buedel B, Convey P et al (2015) Biogeography of photoautotrophs in the high polar biome. Front Plant Sci Funct Plant Ecol 6:692. doi: 10.3389/fpls.2015.00692 Google Scholar
  34. Quince C, Lanzen A et al (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6(9):639–641. doi: 10.1038/nmeth.1361 CrossRefPubMedGoogle Scholar
  35. Quince C, Lanzen A et al (2011) Removing noise from pyrosequenced amplicons. BMC Bioinform. doi: 10.1186/1471-2105-12-38 Google Scholar
  36. Ruisi S, Barreca D, Selbmann L et al (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6:127–141. doi: 10.1007/s11157-006-9107-y CrossRefGoogle Scholar
  37. SCAR (2004) SCAR Bulletin 155. Polar Rec (Gr Brit) 40:371–382. doi: 10.1017/S0032247404003948 CrossRefGoogle Scholar
  38. Schloss PD, Westcott SL et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. doi: 10.1128/AEM.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Smith JJ, Tow LA, Stafford W et al (2006) Bacterial diversity in three different Antarctic Cold Desert mineral soils. Microb Ecol 51:413–421. doi: 10.1007/s00248-006-9022-3 CrossRefPubMedGoogle Scholar
  40. Stomeo F, Makhalanyane TP, Valverde A et al (2012) Abiotic factors influence microbial diversity in permanently cold soil horizons of a maritime-associated Antarctic Dry Valley. FEMS Microbiol Ecol 51:413–421. doi: 10.1111/j.1574-6941.2012.01360.x Google Scholar
  41. Sun LJ, Cai YP et al (2009) ESPRIT: estimating species richness using large collections of 16S rRNA pyrosequences. Nucleic Acids Res 37(10):e76. doi: 10.1093/nar/gkp285 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Tang Y, Lian B et al (2012) Endolithic bacterial communities in dolomite and limestone rocks from the Nanjiang Canyon in Guizhou karst area (China). Geomicrobiol J 29(3):213–225. doi: 10.1080/01490451.2011.558560 CrossRefGoogle Scholar
  43. Thüs H, Muggia L, Pérez-Ortega S, Favero-Longo SE et al (2011) Revisiting photobiont diversity in the family Verrucariaceae (Ascomycota). Eur J Phycol 46:399–415. doi: 10.1080/09670262.2011.629788 CrossRefGoogle Scholar
  44. Valverde A, Makhalanyane TP, Seely M, Cowan DA (2015) Cyanobacteria drive community composition and functionality in rock-soil interface communities. Mol Ecol 24:812–821. doi: 10.1111/mec.13068 CrossRefPubMedGoogle Scholar
  45. Vincent WF, Downes MT, Castenholz RW, Howard-Williams C (1993) Community structure and pigment organisation of cyanobacteria-dominated microbial mats in Antarctica. Eur J Phycol 28:213–221. doi: 10.1080/09670269300650321 CrossRefGoogle Scholar
  46. 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(16):5261–5267. doi: 10.1128/AEM.00062-07 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wierzchos J, Ascaso C (1994) Application of backscattered electron imaging to the study of the lichen-rock interface. J Microsc 175(1):54–59. doi: 10.1111/j.1365-2818.1994.tb04787.x CrossRefGoogle Scholar
  48. Wierzchos J, de los Ríos A, Sancho LG, Ascaso C (2004) Viability of endolithic micro-organisms in rocks from the McMurdo Dry Valleys of Antarctica established by confocal and fluorescence microscopy. J Microsc 216:57–61. doi: 10.1111/j.0022-2720.2004.01386.x CrossRefPubMedGoogle Scholar
  49. Wierzchos J, Sancho LG, Ascaso C (2005) Biomineralization of endolithic microbes in rocks from the McMurdo Dry Valleys of Antarctica: implications for microbial fossil formation and their detection. Env Microbiol 7:566–575. doi: 10.1111/j.1462-2920.2005.00725.x CrossRefGoogle Scholar
  50. Wierzchos J, de los Ríos A, Ascaso C (2012) Microorganisms in desert rocks: the edge of life on Earth. Int Microbiol 15:173–183. doi: 10.2436/20.1501.01.170 PubMedGoogle Scholar
  51. Wong FKY, Lacap DC, Lau MCY et al (2010) Endolithic microbial colonization of limestone in a high-altitude arid environment. Microb Ecol 59:689–699. doi: 10.1007/s00248-009-9607-8 CrossRefPubMedGoogle Scholar
  52. Wynn-Williams DD (1990) Ecological aspects of Antarctic microbiology. In: Advances in microbial ecology. Springer, New York, pp 71–146. doi: 10.1007/978-1-4684-7612-5_3
  53. Yung CCM, Chan Y, Lacap DC et al (2014) Characterization of chasmoendolithic community in Miers Valley, McMurdo Dry Valleys, Antarctica. Microb Ecol 68:351–359. doi: 10.1007/s00248-014-0412-7 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Stephen D. J. Archer
    • 1
    • 2
  • Asuncion de los Ríos
    • 3
  • Kevin C. Lee
    • 1
    • 2
  • Thomas S. Niederberger
    • 2
  • S. Craig Cary
    • 2
    • 4
  • Kathryn J. Coyne
    • 4
  • Susanne Douglas
    • 5
  • Donnabella C. Lacap-Bugler
    • 1
  • Stephen B. Pointing
    • 1
    • 2
    • 6
    Email author
  1. 1.Institute for Applied Ecology New Zealand, School of Applied SciencesAuckland University of TechnologyAucklandNew Zealand
  2. 2.International Centre for Terrestrial Antarctic Research, School of ScienceUniversity of WaikatoHamiltonNew Zealand
  3. 3.Museo Nacional de Ciencias Naturales, CSICMadridSpain
  4. 4.College of Earth, Ocean and EnvironmentUniversity of DelawareLewesUSA
  5. 5.Jet Propulsion LaboratoryCalifornia Institute of TechnologyPasadenaUSA
  6. 6.Institute of Nature and Environmental TechnologyKanazawa UniversityKanazawaJapan

Personalised recommendations