Skip to main content Accessibility help

Sea ice, extremophiles and life on extra-terrestrial ocean worlds

  • Andrew Martin (a1) and Andrew McMinn (a1)


The primary aim of this review is to highlight that sea-ice microbes would be capable of occupying ice-associated biological niches on Europa and Enceladus. These moons are compelling targets for astrobiological exploration because of the inferred presence of subsurface oceans that have persisted over geological timescales. Although potentially hostile to life in general, Europa and Enceladus may still harbour biologically permissive domains associated with the ice, ocean and seafloor environments. However, validating sources of free energy is challenging, as is qualifying possible metabolic processes or ecosystem dynamics. Here, the capacity for biological adaptation exhibited by microorganisms that inhabit sea ice is reviewed. These ecosystems are among the most relevant Earth-based analogues for considering life on ocean worlds because microorganisms must adapt to multiple physicochemical extremes. In future, these organisms will likely play a significant role in defining the constraints on habitability beyond Earth and developing a mechanistic framework that contrasts the limits of Earth's biosphere with extra-terrestrial environments of interest.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Sea ice, extremophiles and life on extra-terrestrial ocean worlds
      Available formats

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Sea ice, extremophiles and life on extra-terrestrial ocean worlds
      Available formats

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Sea ice, extremophiles and life on extra-terrestrial ocean worlds
      Available formats


Corresponding author


Hide All
Anderson, S.P. (2016). Ocean worlds exploration program: new budget calls for missions to Europa, Enceladus and Titan. AmericaSpace. 20th May 2015. Web.
Antia, N.J. (1976). Effects of temperature on the darkness survival of marine microplanktonic algae. Microb. Ecol. 3, 4154.
Arrigo, K.R. (2014). Sea ice ecosystems. Annu. Rev. Mar. Sci. 6, 439467.
Arrigo, K.R. & Sullivan, C.W. (1992). The influence of salinity and temperature covariation on the photophysiological characteristics of Antarctic sea ice microalgae. J. Phycol. 28, 746756.
Arrigo, K.R. & Thomas, D.N. (2004). Large scale importance of sea ice biology in the Southern Ocean. Antarct. Sci. 16, 471486.
Aslam, S.N., Cresswell-Maynard, T., Thomas, D.N. & Underwood, G.J. (2012a). Production and characterisation of the intra- and extracellular carbohydrates and polymeric substances (EPS) of three sea-ice diatom species, and evidence for a cryoprotective role for EPS. J. Phycol. 48, 14941509.
Aslam, S.N. et al. (2012b). Dissolved extracellular polymeric substances (dEPS) dynamics and bacterial growth during sea ice formation in an ice tank study. Polar Biol. 35, 661676.
Azam, F. & Malfatti, F. (2007). Microbial structuring of marine ecosystems. Nat. Rev. Microbiol. 5, 782791.
Bakermans, C. & Skidmore, M. (2011). Microbial respiration in ice at subzero temperatures (−4°C to −33°C). Environ. Microbiol. Rep. 3, 774782.
Bates, N.R. et al. (2014). Sea-ice melt CO2–carbonate chemistry in the western Arctic Ocean: meltwater contributions to air–sea CO2 gas exchange, mixed-layer properties and rates of net community production under sea ice. Biogeosciences 11, 67696789.
Belzile, C. et al. (2000). Ultraviolet attenuation by dissolved and particulate constituents of first-year ice during late spring in an Arctic polyna. Limnol. Oceanogr. 45, 12651273.
Bowman, J.P. (2013). Sea ice microbial communities. In The Prokaryotes: Prokaryotic Communities and Ecophysiology, ed. Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E. & Thompson, F., pp. 193–161. Springer-Verlag, Berlin, Heidelberg.
Bowman, J.S. (2015). The relationship between sea ice bacterial community structure and biogeochemistry: a synthesis of current knowledge and known unknowns. Elem. Sci. Anth. 3, 000072.
Bowman, J.S. & Ducklow, H.W. (2015). Microbial communities can be described by metabolic structure: a general framework and application to a seasonally variable, depth-stratified microbial community from the coastal West Antarctic Peninsula. PLoS ONE 10, e0135868.
Bunt, J.S. & Lee, C.C. (1972). Data on the composition and dark survival of four sea ice algae. Limnol. Oceanogr. 17, 458461.
Casanueva, A. et al. (2010). Molecular adaptations to psychrophily: the impact of ‘omic’ technologies. Trends Microbiol. 18, 374381.
Cavicchioli, R. et al. (2002). Low-temperature extremophiles and their adaptations. Curr. Opin. Biotechnol. 13, 253261.
Celik, Y. et al. (2013). Microfluidic experiments reveal that antifreeze proteins bound to ice crystals suffice to prevent their growth. Proc. Natl. Accad. Sci. USA 110, 13091314.
Chang, W.S. & Halverson, L.J. (2003). Reduced water availability influences the dynamics, development and ultrastructural properties of Pseudomonas putida biofilms. J. Bacteriol. 185, 61996204.
Chang, W.S. et al. (2007). Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J. Bacteriol. 189, 82908299.
Chen, Z., He, C. & Hu, H. (2012). Temperature responses of growth, photosynthesis, fatty acid and nitrate reductase in Antarctic and temperate Stichococcus . Extremophiles 16, 127133.
Chyba, C.F. (2000). Energy for microbial life on Europa. Nature 403, 381382.
Chyba, C.F. & Hand, K.P. (2001). Life without photosynthesis. Science 292, 20262027.
Chyba, C.F. & Phillips, C.B. (2001). Possible ecosystems and the search for life on Europa. Proc. Natl. Acad. Sci. USA 98, 801804.
Chyba, C.F. & Phillips, C.B. (2002). Europa as an abode of life. Orig Life Evol. B 32, 4768.
Chyba, C.F., Whitmire, D.P. & Reynolds, R. (2000). Planetary habitability and the origin of life. In Protostars and Planets IV, ed. Mannings, V., Boss, A.P. & Russell, S.S., pp. 13651393. University of Arizona Press, Tucson, USA.
Cockell, C.S. (2014). Types of habitat in the universe. Int. J. Astrobiol. 13, 158164.
Cockell, C.S. et al. (2016). Habitability: a review. Astrobiology 16, 89117.
Colangelo-Lillis, J., Eicken, H., Carpenter, S.D. & Deming, J.W. (2016). Evidence for marine origin and microbial-viral habitability of sub-zero hypersaline aqueous inclusions within permafrost near Barrow, Alaska. FEMS Microbiol. Ecol. 92. doi: 10.1093/femsec/fiw053. First published online: 13 March 2016.
Collins, T. et al. (2008). Fundamentals of cold-adapted enzymes. In Psychrophiles: from Biodiversity to Biotechnology, ed. Margesin, R., Schinner, F., Marx, J.-C. & Gerday, C., pp. 211227. Springer-Verlag, Berlin, Germany.
Corliss, J.B. et al. (1979). Submarine thermal springs on the Galápagos Rift. Science 203, 10731083.
Cota, G.F. (1985). Photoadaptation of high Arctic algae. Nature 315, 219222.
Cottin, H. et al. (2015). Astrobiology and the possibility of life on Earth and elsewhere. Space Sci. Rev.
Dachwald, B. et al. (2014). IceMole: a maneuverable probe for clean in situ analysis and sampling of subsurface ice and subglacial aquatic ecosystems. Ann. Glaciol. 55, 1422.
Dartnell, L. (2011). Biological constraints on habitability. Astron. Geophys. 52, 1.251.28.
Davies, P.L. (2014). Ice-binding proteins: a remarkable diversity of structures for stopping and starting ice growth. Trends Biomed. Sci. 39, 548555.
Davis, W.L. & McKay, C.P. (1996). Origins of life: a comparison of theories and application to Mars. Orig. Life Evol. Biosph. 26, 6173.
Deamer, D. & Weber, A.L. (2010). Bioenergetcs and life's origins. Cold Spring Harb. Perspect. Biol. 2, a004929.
Decho, A.W. (1990). Microbial exopolymer secretions in ocean environments: their roles(s) in food webs and marine processes. Oceanogr. Mar. Biol. Annu. Rev. 28, 73153.
de Duve, C. (1995). Vital Dust: the Origin and Evolution of Life on Earth. Basic Books, New York, USA.
De Maayer, P. et al. (2014). Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep. 15, 508517.
Delille, B. et al. (2007). Biogas (CO2, O2, dimethylsulfide) dynamics in spring Antarctic fast ice. Limnol. Oceanogr. 52, 13671379.
Deming, J.W. (2002). Psycrophiles and polar regions. Curr. Opin. Microbiol. 5, 301309.
Deming, J.W. & Eicken, H. (2007). Life in ice. In Planets and Life: The Emerging Science of Astrobiology, ed. Sullivan, W.T. & Baross, J.A., pp. 292312. Cambridge University Press, New York.
Devos, N. et al. (1998). RUBISCO adaptation to low temperatures: a comparative study in psychrophilic and mesophilic unicellular algae. J. Phycol. 34, 655660.
Dieckmann, G.S. et al. (1991). The nutrient status in sea ice of the Weddell Sea during winter: effects of sea ice texture and algae. Polar Biol. 11, 449456.
Dieckmann, G.S. et al. (2008). Calcium carbonate as ikaite crystals in Antarctic sea ice. Geophys. Res. Lett. 35, L08501.
Dumont, F., Marechal, P-A. & Gervais, P. (2004). Cell size and water permeability as determining factors for cell viability after freezing at different cooling rates. Appl. Environ. Microbiol. 70, 268272.
Eicken, H. (1992). The role of sea ice in structuring Antarctic ecosystems. Polar Biol. 12, 313.
Ewert, M. & Deming, J.W. (2013). Sea ice microorganisms: environmental constraints and extracellular responses. Biology 2, 603628.
Ewert, M. & Deming, J.W. (2014). Bacterial response to fluctuations and extremes in temperature and brine salinity at the surface of Arctic winter sea ice. FEMS Microbiol. Ecol. 89, 476489.
Feller, G. (2003). Molecular adaptations to cold in psychrophilic enzymes. Cell Mol. Life Sci. 60, 648662.
Feller, G. & Gerday, C. (2003). Psychrophilic enzymes: hot topics in cold adaptation. Nat. Rev. Microbiol. 1, 200208.
Foyer, C.H., Lelandais, M. & Kunert, K.J. (1994). Photooxidative stress in plants. Physiol. Plant. 92, 696717.
Fredrickson, K.A. & Strom, S.L. (2009). The algal osmolyte DMSP as a microzooplankton grazing deterrent in laboratory and field trials. J. Plank. Res. 31, 135152.
Fritsen, C.H. et al. (2001). Biomass, production and microhabitat characteristics near the freeboard of ice floes in the Ross Sea, Antarctica, during the austral summer. Ann. Glaciol. 33, 280286.
Gaidos, E.J. & Nimmo, F. (2000). Planetary science: tectonics and water on Europa. Nature 405, 637.
Gaidos, E.J., Nealson, K.H. & Kirschvink, J.L. (1999). Life in ice-covered oceans. Science 284, 16311633.
Garrison, D.L. (1991). Antarctic sea ice biota. Amer. Zool. 31, 1733.
Gerday, C. (2013). Psychrophily and catalysis. Biology 2, 719741.
Gerday, C. et al. (2000). Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol. 18, 103107.
Gilbert, J.A. et al. (2004). Demonstration of antifreeze protein activity in Antarctic lake bacteria. Microbiology 150, 171180.
Gilichinsky, D., Rivkina, E., Shcherbakova, V., Laurinavichuis, K. & Tiedje, J. (2003). Supercooled water brines within permafrost – an unknown ecological niche for microorganisms: a model for astrobiology. Astrobiology 3, 331341.
Glein, C.R., Baross, J.A. & Waite, J.H. Jr. (2015). The pH of Enceladus’ ocean. Geochim. Cosmochim. Acta 162, 202219.
Glud, R.N. et al. (2013). High rates of microbial turnover in sediments in the deepest oceanic trench on Earth. Nat. Geosci. 6, 284288.
Greenburg, R. et al. (2000). Habitability of Europa's crust: the role to tidal-tectonic processes. J. Geophys. Res. 105, 1755117562.
Günther, S., Gleitz, M. & Dieckmann, G.S. (1999). Biogeochemistry of Antarctic sea ice: a case study on platelet ice layers at Drescher Inlet, Weddell Sea. Mar. Ecol. Progr. Ser. 177, 113.
Häder, D-P. et al. (2015). Effects of UV radiation on aquatic ecosystems and interactions with other environmental factors. Photochem. Photobiol. Sci. 14, 108126.
Hand, K.P. & Brown, M.E. (2013). Keck II observations of hemispherical differences in H2O2 on Europa. Astrophys. J. Lett. 766, L21.
Hand, K.P. & Chyba, C.F. (2007). Empirical constraints on the salinity of the Europan ocean and implications for a thin ice shell. Icarus 189, 424438.
Hand, K.P., Carlson, R.W. & Chyba, C.F. (2007). Energy, chemical disequilibrium and geological constraints on Europa. Astrobiology 7, 10061022.
Hare, A.A. et al. (2013). pH evolution in sea ice grown at an outdoor experimental facility. Mar. Chem. 154, 4654.
Harrison, J.P. et al. (2013). The limits for life under multiple extremes. Trends Microbiol. 21, 204212.
Hart, M.H. (1978). The evolution of the atmosphere of the Earth. Icarus 33, 2339.
Hébraud, M. & Potier, P. (1999). Cold shock response to low temperature adaptation in psychrotrophic bacteria. J. Mol. Microbiol. Biotechnol. 1, 211219.
Hoover, R.B. & Pikuta, E.V. (2009). Psychrophilic and psychrotolerant microbial extremophiles in polar environments. In Polar Microbiology: The Ecology, Biodiversity and Bioremediation Potential of Microorganisms in Extremely Cold Environments, ed. Bej, A.K., Aislabie, J. & Atlas, R.M., pp. 115156. CRC Press, USA.
Horneck, G., Klaus, D.M. & Mancinelli, R.L. (2010). Space microbiology. Microbiol. Mol. Biol. R 74, 121156.
Horner, R.A. & Alexander, V. (1972). Algal populations in Arctic sea ice: an investigation of heterotrophy. Limnol. Oceanogr. 17, 454458.
Hoyle, F. et al. (1982). Infrared spectroscopy of micro-organisms near 3,4 m in relation to geology and astronomy. Astrophys. Space Sci. 81, 489492.
Hsu, H-W. et al. (2015). Ongoing hydrothermal activities within Enceladus. Nature 519, 207210.
Hünken, M., Harder, J. & Kirst, G.O. (2008). Epiphytic bacteria on the Antarctic diatom Amphiphora kufferathii Manguin cleave hydrogen peroxide produced during algal photosynthesis. Plant Biol. 10, 519526.
Huston, A.L., Krieger-Brockett, B.B. & Deming, J.W. (2000). Remarkably low temperature optima for extracellular enzyme activity from Arctic bacteria and sea ice. Environ. Microbiol. 2, 38388.
Janknegt, P.J. et al. (2008). Oxidative stress responses in the marine Antarctic diatom Chaetoceros brevis (Bacillariophyceae) during photoacclimation. J. Phycol. 44, 957966.
Junge, K. et al. (2002). Phylogenetic diversity of numerically important Arctic sea-ice bacteria cultured at subzero temperatures. Microb. Ecol. 43, 315328.
Kargel, J.S. et al. (2000). Europa's crust and ocean: origin, composition, and the prospects for life. Icarus 148, 226265.
Kasting, J.F., Whitmire, D.P. & Reynolds, R.T. (1993). Habitable zones around main sequence stars. Icarus 101, 108128.
Kattenhorn, S.A. & Prockter, L.M. (2014). Evidence for subduction in the ice shell of Europa. Nat. Geosci. 7, 762767.
Kelley, D.S. et al. (2001). An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30°N. Nature 412, 145149.
Kerr, R.A. (2001). Putting a lid on life on Europa. Science 294, 12581259.
King, M.D. et al. (2005). Measurement and modelling of UV radiation penetration and photolysis rates of nitrate and hydrogen peroxide in Antarctic sea ice: an estimate of the producton rate of hydroxyl radicals in first-year sea ice. J. Phytochem. Photobiol. A 176, 3949.
Kloster, S. et al. (2006). DMS cycle in the marine ocean-atmosphere system – a global model study. Biogeosciences 3, 2951.
Koh, Y.E. et al. (2012). Recent advances and future perspectives in microbial phototrophy in Antarctic sea ice. Biology 1, 542556.
Kottmeier, S.T. & Sullivan, C.W. (1988). Sea ice microbial communities (SIMCO): effects of temperature and salinity on rates of metabolism and growth of autotrophs and heterotrophs. Polar Biol. 8, 293304.
Krell, A. et al. (2007). Regulation of proline metabolism under salt stress in the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). J. Phycol. 43, 753762.
Krembs, C. & Deming, J.W. (2008). The role of exopolymers in microbial adaptation to sea ice. In Psychrophiles: from Biodiversity to Biotechnology, ed. Margesin, R., Schinner, F., Marx, J.-C. & Gerday, C., pp. 247264. Springer-Verlag, Berlin, Germany.
Krembs, C., Eicken, H., Junge, K. & Deming, J.W. (2002). High concentrations of exopolymeric substances in Arctive winter sea ice: implication for the polar ocean carbon cycle and cryoprotection of diatoms. Deep-Sea Res. I 49, 21632181.
Krembs, C., Eicken, J. & Deming, J.W. (2011). Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc. Natl. Acad. Sci. USA 108, 36533658.
Lederberg, J. (1960). Exobiology: approaches to life beyond the Earth. Science 132, 393400.
Legrand, C., Graneli, E. & Carlson, P. (1998). Induced phagotrophy in the photosynthetic dinoflagellate Heterocapsa triquetra . Aquat. Microb. Ecol. 15, 6575.
Lin, L-H. et al. (2006). Long-term sustainability of a high-energy, low-diversity crustal biome. Science 314, 479482.
Lizotte, M.P. & Sullivan, C.W. (1992). Biochemical composition and photosynthate distribution in sea ice microalgae of McMurdo Sound, Antarctica: evidence for nutrient stress during the spring bloom. Antarct. Sci. 4, 2330.
Lorv, J.S.H., Rose, D.R. & Glick, B.R. (2014). Bacterial ice crystal controlling proteins. Scientifica 2014, 976895.
Lyon, B.R. & Mock, T. (2014). Polar microalgae: new approaches towards understanding adaptations to an extreme and changing environment. Biology 3, 5680.
Mallick, N. & Mohn, F.H. (2000). Reactive oxygen species: response of algal cells. J. Plant Physiol. 157, 183193.
Margesin, R. & Miteva, V. (2011). Diversity and ecology of psychrophilic microorganisms. Res. Microbiol. 162, 346361.
Marlin, G. & Kirst, G.O. (1997). Algal production of dimethyl sulphide and its atmospheric role. J. Phycol. 33, 889896.
Martin, A., Hall, J.A. & Ryan, K.G. (2009). Low salinity and high-level UV-B radiation reduce single-cell activity in Antarctic sea ice bacteria. Appl. Environ. Microbiol. 75, 75707573.
Martin, A. et al. (2012). The physiological response to increased temperature by over-wintering sea ice algae and phytoplankton in McMurdo Sound, Antarctica and Tromsø Sound, Norway. J. Exp. Mar. Biol. Ecol. 428, 5766.
Martin, W., Baross, J., Kelley, D. & Russell, M.J. (2008). Hydrothermal vents and the origin of life. Nat. Rev. Microbiol. 6, 805814.
Marx, J-C. et al. (2007). Cold-adapted enzymes from marine Antarctic organisms. Mar. Biotechnol. 9, 293304.
Maxwell, D.P. et al. (1994). Growth at low temperature mimics high-light acclimation in Chlorella vulgaris . Plant Physiol. 105, 535543.
McCliment, E.A. et al. (2006). Colonisation of nascent, deep-sea hydrothermal vents by a novel archaeal and nanoarchaeal assemblage. Environ. Microbiol. 8, 114125.
McKay, C.P. (2014). Requirements and limits for life in the context of exoplanets. Proc. Natl. Acad. Sci. USA 111, 1262812633.
McMinn, A. & Martin, A. (2013). Dark survival in a warming world. Proc. R. Soc. B 280, 20122909.
McMinn, A., Heijnis, H. & Hodgson, D. (1994). Minimal effects of UV-B on Antarctic diatoms over the past 20 years. Nature 370, 547549.
McMinn, A., Ashworth, C. & Ryan, K.G. (1999a). Growth and productivity of Antarctic sea ice algae under PAR and UV irradiances. Bot. Mar. 42, 401407.
McMinn, A. et al. (1999b). Nutrient stress gradient in the bottom 5 cm of fast ice, McMurdo Sound, Antarctica. Polar Biol. 21, 220227.
McMinn, A., Ryan, K.G. & Gademann, R. (2003). Diurnal changes in photosynthesis of Antarctic fast ice algal communities determined by pulse amplitude modulation fluorometry. Mar. Biol. 143, 359367.
McMinn, A., Pankowski, A. & Delfatti, T. (2005). Effect of hyperoxia on the growth and photosynthesis of polar sea ice microalgae. J. Phycol. 41, 732741.
McMinn, A., Martin, A. & Ryan, K.G. (2010). Phytoplankton and sea ice algal biomass and physiology during the transition between winter and spring (McMurdo Sound, Antarctica). Polar Biol. 33, 15471556.
McMinn, A. et al. (2014). The response of Antarctic sea ice algae to changes in pH and CO2 . PLoS ONE 9, e86984.
Meador, J. et al. (2002). Seasonal fluctuation of DNA photodamage in marine plankton assemblages at Palmer Station, Antarctica. Photochem. Photobiol. 75, 266271.
Melosh, H.J. et al. (2004). The temperature of Europa's subsurface water ocean. Icarus 168, 498502.
Methé, B.A. et al. (2005). The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc. Natl. Acad. Sci. USA 102, 1091310918.
Mock, T. (2002). In situ primary production in young Antarctic sea ice. Hydrobiology 470, 127132.
Mock, T. & Hoch, N. (2005). Long-term temperature acclimation of photosynthesis in steady-state cultures of the polar diatom Fragilariopsis cylindrus . Photosynth. Res. 85, 307317.
Mock, T. & Kroon, B.M.A. (2002). Photosynthetic energy conversion under extreme conditions I: important role of lipids as structural modulators and energy sink under N-limited growth in Antarctic sea ice diatoms. Phytochemistry 61, 4151.
Mock, T. & Thomas, D.N. (2005). Recent advances in sea-ice microbiology. Environ. Microbiol. 7, 605619.
Moorthi, S. et al. (2009). Mixotrophy: a widespread and important ecological strategy for planktonic and sea-ice nanoflagellates in the Ross Sea, Antarctica. Aquat. Microb. Ecol. 54, 269277.
Morgan-Kiss, R.M. et al. (2006). Adaptation and acclimation of phytosynthetic microorganisms to permanently cold environments. Microbiol. Mol. Biol. R 70, 222252.
Murray, A.E. et al. (2012). Microbial life at −13°C in the brine of an ice-sealed Antarctic lake. Proc. Natl. Acad. Sci. USA 109, 2062620631.
Nagy, M.L., Perez, A. & Garcia-Pichel, F. (2005). The prokaryotic diversity of biological soil crusts in the Sonorian Desert (Organ pipe cactus national monument, AZ). FEMS Microbiol. Ecol. 54, 233245.
Nedwell, D.B. (1999). Effect of low temperature on microbial growth: lowered affinity for substrates limits growth at low temperature. FEMS Microbiol. Ecol. 30, 101111.
Nichols, D. et al. (1999). Developments with Antarctic microorganisms: culture collections, bioactivity screening, taxonomy, PUFA production and cold-adapted enzymes. Curr. Opin. Biotechnol. 10, 240246.
Nimmo, F. & Manga, M. (2009). Geodynamics of Europa's icy shell. In Europa, ed. Pappalardo, R., McKinnon, W. & Khurana, K., pp. 381404. Arizona Press Space Science Series, USA.
Nimmo, F. et al. (2007). Shear heating as the origin of the plumes and heat flux on Enceladus. Nature 447, 289291.
Nishiguchi, M.K. & Somero, G.N. (1992). Temperature - and concentration-dependence of compatibility of the organic osmolyte β-dimethylsulfoniopropionate. Cryobiology 29, 118124.
Ozturk, S. & Aslim, B. (2010). Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environ. Sci. Pollut. Res. 17, 595602.
Pace, N.R. (1997). A molecular view of microbial diversity and the biosphere. Science 276, 734740.
Palmisano, A.C. & Sullivan, C.W. (1983). Sea ice microbial communities (SIMCO) 1. Distribution, abundance, and primary production of ice microalgae in McMurdo Sound, Antarctica in 1980. Polar Biol. 2, 171177.
Parkinson, C.D. et al. (2008). Habitability of Enceladus: planetary conditions for life. Orig. Life Evol. Biosph. 38, 355369.
Parkinson, C.L. (2014). Global sea ice coverage from satellite data: annual cycle and 35-yr trends. J. Clim. 27, 93779382.
Paterson, H. & Laybourn-Parry, J. (2012). Sea ice microbial dynamics over an annual ice cycle in Prydz Bay, Antarctica. Polar Biol. 35, 9931002.
Peck, L.S. (2005). Prospects for surviving climate change in Antarctic aquatic species. Front. Zool. 2, 29.
Pedrós-Alió, C. (2006). Marine microbial diversity: can it be determined? Trends Microbiol. 14, 257263.
Perovich, D.K. (1993). A theoretical model of ultraviolet light transmission through Antarctic sea ice. J. Geophys. Res. 98, 2257922587.
Phadtare, S. (2004). Recent developments in bacterial cold-shock response. Curr. Issues Mol. Biol. 6, 125136.
Pomeroy, L.R. & Wiebe, W.J. (2001). Temperature and substrates as interactive limiting factors for marine heterotrophic bacteria. Aquat. Microb. Ecol. 23, 187204.
Pomeroy, L.R. et al. (2007). The microbial loop. Oceanography 20, 2833.
Porco, C., DiNino, D. & Nimmo, F. (2014). How the geysers, tidal stress, and thermal emission across the south polar terrain of Enceladus are related. Astron. J. 148, 45.
Postberg, F. et al. (2009). Sodium salts in E-ring ice giants from an ocean below the surface of Enceladus. Nature 459, 10981101.
Postberg, F. et al. (2011). A salt-water reservoir as the source of a compositionally stratified plume on Enceladus. Nature 474, 620622.
Ralph, P.J. et al. (2005). Short-term effect of temperature on the photokinetics of microalgae from the surface layers of Antarctic pack ice. J. Phycol. 41, 763769.
Ralph, P.J. et al. (2007). Melting out of sea ice causes greater photosynthetic stress in algae than freezing in. J. Phycol. 43, 948956.
Raymond, J.A. (2014). The ice-binding proteins of a snow alga, Chloromanas brevispina: probable acquisition by horizontal gene transfer. Extremophiles 18, 987994.
Raymond, J.A. & Kim, H.J. (2012). Possible role of horizontal gene transfer in the colonisation of sea ice by algae. PLoS ONE 7, e35968.
Raymond, J.A. & Knight, C.A. (2003). Ice binding, recrystallization inhibition, and cryoprotective properties of ice-active substances associated with Antarctic sea ice diatoms. Cryobiology 46, 174181.
Riedel, A. et al. (2007). Enrichment of nutrients, exopolymeric substances and microorganisms in newly formed sea ice on the Mackenzie shelf. Mar. Ecol. Progr. Ser. 342, 5567.
Rivkin, R.B. & Putt, M. (1987). Heterotrophy and photoheterotrophy by Antarctic microalgae: light-dependent incorporation of amino acids and glucose. J. Phycol. 23, 442452.
Roberts, M.F. (2005). Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst. 1, 5.
Roth, L. et al. (2014). Transient water vapour at Europa's south pole. Science 343, 171174.
Rothschild, L.J. & Mancinelli, R.L. (2001). Life in extreme environments. Nature 409, 10921101.
Runnegar, B. (1992). Evolution of the earliest animals. In Major Events in the History of Life, ed. Schopf, J.W., pp. 6593. Jones & Barlett Publishers, Boston, USA.
Russell, N.J. (1997). Psychrophilic bacteria – molecular adaptations of membrane lipids. Comp. Biochem. Physiol. 118A, 489493.
Russell, N.J. (2000). Toward a molecular understanding of cold activity of enzymes from psychrophiles. Extremophiles 4, 8390.
Russell, N.J. & Nichols, D.S. (1999). Polyunsaturated fatty acids in marine bacteria – a dogma rewritten. Microbiology 145, 767779.
Ryan, K.G. (1992). UV radiation and photosynthetic production in Antarctic sea ice microalgae. J. Photochem. Photobiol. B: Biol. 13, 235240.
Ryan, K.G., Ralph, P. & McMinn, A. (2004). Acclimation of Antarctic bottom-ice algal communities to lowered salinities during melting. Polar Biol. 27, 679686.
Ryan, K.G. et al. (2012). The effects of ultraviolet-B radiation on Antarctic sea ice algae. J. Phycol. 48, 7484.
Rysgaard, S. et al. (2014). Temporal dynamics in ikaite in experimental sea ice. Cryosphere 8, 14691478.
Schmidt, B.E. et al. (2011). Active formation of ‘chaos terrain’ over shallow subsurface water on Europa. Nature 479, 502505.
Schmidt, J. et al. (2008). Slow dust in Enceladus’ plume from condensation and wall collisions in tiger stripe features. Nature 451, 685688.
Schriek, R. (2000). Effects of light and temperature on the enzymatic antioxidative defence systems in the Antarctic ice diatom Entomoneis kufferathii . Ber. Polarforsch. 349, 1129.
Schubert, G. et al. (2010). Evolution of icy satellites. Space Sci. Rev. 153, 447484.
Sekine, Y. et al. (2015). High-temperature water-rock interactions and hydrothermal environments in the chondrite-like core of Enceladus. Nat. Commun. 6, 8604. doi: 10.1038/ncomms9604.
Shivaji, S. & Prakash, J.S.S. (2010). How do bacteria sense and respond to low temperature? Arch. Microbiol. 192, 8595.
Siddiqui, K.S. & Cavicchioli, R. (2006). Cold-adapted enzymes. Annu. Rev. Biochem. 75, 403433.
Sievert, S.M., Kiene, R.P. & Schulz-Vogt, H.N. (2007). The sulfur cycle. Oceanography 20, 117123.
Soo, R.M. et al. (2009). Microbial biodiversity of thermophilic communities in hot mineral soils of Tramway Ridge, Mount Erebus, Antarctica. Environ. Microbiol. 11, 715728.
Spencer, J.R. & Nimmo, F. (2013). Enceladus: an active ice world in the Saturn system. Annu. Rev. Earth Planet Sci. 41, 693717.
Spiess, F.N. et al. (1980). East Pacific Rise: hot springs and geophysical experiments. Science 207, 14211433.
Staley, J.T. & Gosink, J.J. (1999). Poles apart: biodiversity and biogeography of sea ice bacteria. Annu. Rev. Microbiol. 53, 189215.
Steele, D.J., Franklin, D.J. & Underwood, G.J.C. (2014). Protection of cells from salinity stress by extracellular polymeric substances in diatom biofilms. Biofouling 30, 987998.
Stevens, T.O. & McKinley, J.P. (1995). Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science 270, 450454.
Stevenson, A. et al. (2015). Multiplication of microbes below 0.690 water activity: implications for terrestrial and extraterrestrial life. Environ. Microbiol. 17, 257277.
Stewart, F.J. & Fritsen, C.H. (2004). Bacteria-algae relationships in Antarctic sea ice. Antarct. Sci. 16, 143156.
Struvay, C. & Feller, G. (2012). Optimization to low temperature activity in psychrophilic enzymes. Int. J. Mol. Sci. 13, 1164311665.
Stüeken, E.E. et al. (2013). Did life originate from a global chemical reactor? Geobiology 11, 101126.
Sunda, W. et al. (2002). An antioxidant function for DMSP and DMS in marine algae. Nature 418, 317320.
Taylor, F. & McMinn, A. (2002). Late quaternary diatom assemblages from Prydz Bay, Eastern Antarctica. Quat. Res. 57, 151161.
Thomas, D.N. & Dieckmann, G.S. (2002a). Antarctic sea ice – a habitat for extremophiles. Science 295, 641644.
Thomas, D.N. & Dieckmann, G.S. (2002b). Biogeochemistry of Antarctic sea ice. Oceanogr. Mar. Biol. 40, 143169.
Thomas, D.N. & Papadimitriou, S. (2003). Biogeochemistry of sea ice. In Sea Ice – an Introduction to its Physics, Biology and Geology, ed. Thomas, D.N. & Dieckmann, G.S., pp. 267302. Blackwell Publishing, Oxford Publishing, Oxford, UK.
Thomas, P.C. et al. (2015). Enceladus's measured physical libration requires a global subsurface ocean. Icarus 264, 3747.
Thomson, P.G. et al. (2004). Antarctic distribution, pigment and lipid composition, and molecular identification of the brine dinoflagellate Polarella glacialis (Dinophyceae). J. Phycol. 40, 867873.
Torstensson, A. et al. (2013). Synergism between elevated pCO2 and temperature on the Antarctic sea ice diatom Nitzschia lecointei . Biogeosciences 10, 63916401.
Travis, B.J., Palguta, J. & Schubert, G. (2012). A whole-moon thermal history model of Europa: impact of hydrothermal circulation and salt transport. Icarus 218, 10061019.
Trodahl, H.J. & Buckley, R.G. (1990). Enhanced ultraviolet transmission of Antarctic sea ice during the austral spring. Geophys. Res. Lett. 17, 21772179.
Ugalde, S. et al. (2014). Extracellular organic carbon dynamics during a bottom-ice algal bloom (Antarctica). Aquat. Microb. Ecol. 73, 195210.
Ulig, C. et al. (2015). In situ expression of eukaryotic ice-binding proteins in microbial communities of Arctic and Antarctic sea ice. ISME J. 9, 25372540.
Underwood, G.J.C. et al. (2010). Distribution and composition of dissolved extracellular polymeric substances (EPS) in Antarctic sea ice. Mar. Ecol. Progr. Ser. 404, 119.
Underwood, G.J.C. et al. (2013). Broad-scale predictability of carbohydrates and exopolymers in Antarctic and Arctic sea ice. Proc. Natl. Acad. Sci. USA 110, 1573415739.
van Dokkum, P.G. & Conroy, C. (2010). A substantial population of low-mass stars in luminous elliptical galaxies. Nature 468, 940942.
Vanlindt, D. et al. (2011). Rapid acquisition of gigapascal-high-pressure resistance by Escherichia coli . mBio 2, e00130-10.
Vaqué, D. et al. (2002). Spatial distribution of microbial biomass and activity (bacterivory and bacterial production) in the northern Weddell Sea during the austral summer (January 1994). Aquat. Microb. Ecol. 29, 107121.
Welsh, D.T. (2000). Ecological significance of compatible solute accumulation by micro-organisms: from single cell to global climate. FEMS Microbiol. Rev. 24, 263290.
Werner, I., Ikavalko, J. & Schunemann, H. (2007). Sea ice algae in Arctic pack ice during late winter. Polar Biol. 30, 14931504.
White, P.L., Wynn-Williams, D.D. & Russell, N.J. (2000). Diversity of thermal responses of lipid composition in the membranes of the dominant culturable members of an Antarctic fellfield soil bacterial community. Antarct. Sci. 12, 386393.
Whitman, W.B., Coleman, D.C. & Wiebe, W.J. (1998). Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. USA 95, 65786583.
Young, J.N. et al. (2015a). Slow carboxylation of Rubisco constrains the rate of carbon fixation during Antarctic phytoplankton blooms. New Phytol. 205, 172181.
Young, J.N. et al. (2015b). Antarctic phytoplankton down-regulate their carbon-concentrating mechanisms under high CO2 with no change in growth rates. Mar. Ecol. Progr. Ser. 532, 1328.


Related content

Powered by UNSILO

Sea ice, extremophiles and life on extra-terrestrial ocean worlds

  • Andrew Martin (a1) and Andrew McMinn (a1)


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.