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Microbial ecology of the cryosphere: sea ice and glacial habitats

Key Points

  • Active, diverse microorganisms have been detected in all cryospheric habitats on Earth, and they are as abundant as those living in freshwater habitats.

  • Numerous intracellular and extracellular adaptations enable microorganisms to thrive at temperatures below 0 °C, and thus to survive and grow in liquid inclusions within porous ice matrices.

  • The many different types of cryospheric habitats pose distinct habitability challenges to resident microorganisms. Communities specialized to each type of ice environment use different strategies to fulfil their energy and growth requirements, using either sunlight, or inorganic or organic compounds as energy sources.

  • Today, the use of next-generation sequencing approaches enables more detailed insights into microbial community composition and function, and allows the tracking of structural and functional differences and changes at a high resolution.

  • Climate change is altering the cryosphere; it is expected that this will lead to shifts in the distribution, composition and activity of cold-adapted microorganisms.

Abstract

The Earth's cryosphere comprises those regions that are cold enough for water to turn into ice. Recent findings show that the icy realms of polar oceans, glaciers and ice sheets are inhabited by microorganisms of all three domains of life, and that temperatures below 0 °C are an integral force in the diversification of microbial life. Cold-adapted microorganisms maintain key ecological functions in icy habitats: where sunlight penetrates the ice, photoautotrophy is the basis for complex food webs, whereas in dark subglacial habitats, chemoautotrophy reigns. This Review summarizes current knowledge of the microbial ecology of frozen waters, including the diversity of niches, the composition of microbial communities at these sites and their biogeochemical activities.

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Figure 1: The cryosphere's frozen water realms.
Figure 2: Biogeochemical processes in frozen water ecosystems.
Figure 3: Bacterial composition of the cryosphere.

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Acknowledgements

Support was received from the European Research Council (ERC) Adv G (grant 294757 to A.B.), the Natural Environment Research Council (NERC; grant NE/J02399X/1 to A.M.A.), and the National Science Foundation (NSF; grant ARC-1203267 to J.W.D. and grant ANT-1144178 to J.A.M.).

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Glossary

Psychrophilic

Organisms that thrive at low temperatures. From the Greek words psychrós (ψυχρός) meaning cold, and phílos (φίλος) meaning loving.

Extracellular polymeric substances

(EPS). High-molecular-weight, carbohydrate-rich exudates that are released by microorganisms in response to a shift in environmental conditions, including temperature, salinity and nutrient availability. EPS are composed primarily of polysaccharides but can also include proteins, DNA or lipopolysaccharides.

Aquifer

A body of permeable rock that can contain or transmit groundwater.

Albedo

A measure of how much solar energy a surface reflects, whereby light-coloured surfaces such as sea ice reflect more solar energy than dark surfaces such as open water. Dust particles and pigmentation by algal growth on the surface of ice lower albedo by decreasing ice reflectivity.

Cryoconite holes

Small holes (submetre scale) in the ablation zone on glacial ice surfaces. They form as a result of the deposition of cryoconite (a mixture of dark-coloured inorganic and organic particles, including microorganisms), which absorbs solar radiation and causes the ice to melt.

Ablation zones

Areas of a glacier or ice sheet where ice loss (caused by melting, sublimation, evaporation or ice calving) exceeds ice gain (due to snow accumulation).

Accretion ice

Ice that forms when liquid water freezes to the base of a glacier or ice sheet. An example is lake water from Lake Vostok, which has frozen to the base of the ice sheet, forming a layer of accretion ice.

Basal sediments

The loose debris that is produced by glacial erosion of the underlying material at the icebedrock interface of a glacier or ice sheet.

Brine

Salt-rich liquid trapped in channels and pockets within the ice matrix. In very cold sea ice, some sea salts approach saturating levels and precipitate.

Algal mats

A dense accumulation of phototrophic eukaryotic microorganisms, which grow, for example, on the underside of sea ice.

Foraminifera

A group of single-celled eukaryotes with a characteristic calcium carbonate shell and either a planktonic or benthic lifestyle. The remains of their calcareous fossils in seafloor sediments have important roles in paleoclimatology and paleooceanography.

Sympagic meiofauna

Small animals of <1mm in size that inhabit sea ice.

Diatoms

Unicellular algae, with silicate walls, that constitute the major fraction of phytoplankton in most coastal and polar oceans; they are also the dominant primary producers in sea ice.

Grazing pressure

Stress on a population of organisms due to grazing or consumption by other, typically larger organisms.

Proteorhodopsin

A photoactive protein that functions as a light-driven proton pump and is used by some marine microorganisms to generate additional energy.

Polyunsaturated fatty acids

(PUFAs). Lipids that contain carbon backbones with two or more carboncarbon double bonds. They are unsaturated with respect to the number of hydrogen atoms per carbon atom.

Seed communities

The source of organisms to a transient ecosystem.

Glacial runoff

The meltwater draining from glaciers and ice sheets that may come from both surface (supraglacial) and subsurface (subglacial) melt.

Glacier forefields

The terrain most recently exposed by a retreating glacier. This region lies between the current terminus or leading edge of a glacier and the accumulation of glacial debris that marks the previous (greater) extent of the glacier.

Bedrock

The deeper layer of consolidated rock that underlies loose materials, such as soil, gravel and sediment.

Chemolithoautotrophs

Organisms that gain their energy through the oxidation of reduced inorganic compounds and use CO2 as the sole carbon source for growth. The term is often used synonymously with chemoautotrophy and chemosynthesis.

Heterotrophs

Organisms that use organic compounds as their carbon source and obtain energy through the oxidation of these compounds.

Redox chemistry

Pairs of reactions in which one compound becomes oxidized and releases electrons, and the other compound becomes reduced and accepts the released electrons.

Remotely operated vehicles

(ROVs). Tethered unmanned underwater robots often used for deep-water research or industrial purposes.

Methanogenesis

The biological production of methane (CH4) in an anaerobic process mediated exclusively by methanogenic archaea.

Phylotypes

Different taxonomic groups of microorganisms that can be determined by comparative analyses of their 16S rRNA gene sequences.

Calvin cycle

A series of biochemical reactions used by many photosynthetic organisms to convert CO2 into organic compounds.

Isotopic signature

The ratio of isotopes of a particular element in a molecule of interest, as measured by isotope ratio mass spectrometry.

Ice-binding proteins

Proteins used by microorganisms to prevent or limit the growth of ice structures within or outside of their body fluids, by, for example, adhering to the ice or otherwise inhibiting ice crystal growth or recrystallization.

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Boetius, A., Anesio, A., Deming, J. et al. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat Rev Microbiol 13, 677–690 (2015). https://doi.org/10.1038/nrmicro3522

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