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.
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References
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Friedmann EI (1980) Endolithic microbial life in hot and cold deserts. Orig Life 10:223–235
Friedmann EI (1982) Endolithic microorganisms in the antarctic cold desert. Science 215:1045–1053. doi:10.1126/science.215.4536.1045
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
Friedmann E, Hua M, Ocampo-Friedmann R (1988) Cryptoendolithic lichen and cyanobacteria communities of the Ross Desert, Antarctica. Polarforschung 58:251–259
Gao Q, Garcia-Pichel F (2011) Microbial ultraviolet sunscreens. Nat Rev Micro 9:791–802. doi:10.1038/nrmicro2649
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
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
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
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
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
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
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
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
Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Micro 10:551–562. doi:10.1038/nrmicro2831
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
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
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
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
Quince C, Lanzen A et al (2011) Removing noise from pyrosequenced amplicons. BMC Bioinform. doi:10.1186/1471-2105-12-38
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
SCAR (2004) SCAR Bulletin 155. Polar Rec (Gr Brit) 40:371–382. doi:10.1017/S0032247404003948
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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).
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Archer, S.D.J., de los Ríos, A., Lee, K.C. et al. Endolithic microbial diversity in sandstone and granite from the McMurdo Dry Valleys, Antarctica. Polar Biol 40, 997–1006 (2017). https://doi.org/10.1007/s00300-016-2024-9
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DOI: https://doi.org/10.1007/s00300-016-2024-9