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The microbial ecology of permafrost

Key Points

  • Permafrost is a unique habitat for cold-adapted microbial life on Earth and is a model environment for extraterrestrial biomes.

  • Permafrost microorganisms have several strategies for survival under cold conditions.

  • Different permafrost habitats in the Arctic and Antarctica harbour a diversity of microorganisms, many of which exhibit activity at subzero temperatures.

  • Permafrost thaw results in different types of landscape features that can influence microbial composition and activity.

  • Much of the current knowledge of permafrost microbiology was obtained from the study of permafrost isolates, but recent advances in high-throughput sequencing technologies have enabled the detailed exploration of permafrost microbial communities without the necessity for cultivation.

  • The microbial ecology of permafrost is the focus of intensifying interest, owing to the uncertainty of the effects of climate change on the microbial cycling of carbon that is currently sequestered in permafrost.

Abstract

Permafrost constitutes a major portion of the terrestrial cryosphere of the Earth and is a unique ecological niche for cold-adapted microorganisms. There is a relatively high microbial diversity in permafrost, although there is some variation in community composition across different permafrost features and between sites. Some microorganisms are even active at subzero temperatures in permafrost. An emerging concern is the impact of climate change and the possibility of subsequent permafrost thaw promoting microbial activity in permafrost, resulting in increased potential for greenhouse-gas emissions. This Review describes new data on the microbial ecology of permafrost and provides a platform for understanding microbial life strategies in frozen soil as well as the impact of climate change on permafrost microorganisms and their functional roles.

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Figure 1: Changes in landscape caused by permafrost thaw and cryoperturbation.
Figure 2: Permafrost thaw features at lowland and highland elevations.
Figure 3: Microbial composition of permafrost from different geographical locations.

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Acknowledgements

This manuscript is dedicated to the late David Gilichinsky for his research on permafrost microbiology. This work was supported by US Department of Energy (DOE) contract DE-AC02-05CH11231 to Lawrence Berkeley National Laboratory (LBNL), University of California, USA. The authors acknowledge financial support from the DOE-Next Generation Ecosystem Experiment (NGEE-Arctic) and the Danish Center for Permafrost (CENPERM). The authors thank L. Øvreås, University of Bergen, Norway, for critical reading of the manuscript.

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Permafrost isolates and characteristics of interest (PDF 437 kb)

Glossary

Yedoma

A permafrost type that is mainly found in Northeast Siberia. It is characterized by high levels of organic material and up to 90% ice content. Carbon that is trapped in this permafrost is suggested to be susceptible to microbial decomposition following thaw, resulting in the potential release of large quantities of greenhouse gases into the atmosphere.

Cryopegs

Permafrost zones that have high dissolved-solids contents (for example, a high salt concentration in the pore water), thus depressing the freezing point of water.

Talik

A layer of unfrozen ground that can occur in permafrost zones underlying thermokarst lakes and rivers.

Frost mounds

Hummocks or knolls that are produced by freezing combined with groundwater formation through soil in a permafrost region. Frost mounds contain a core of ice that is covered by a thin soil layer.

Thermokarst lakes

(Also known as thaw lakes). Shallow, freshwater bodies that are formed by the collapse of the underlying permafrost and the accumulation of meltwater as permafrost thaws in depression areas.

Frost boils

Sparsely vegetated circular features (with a diameter of 0.5–3 m) on the land surface; they are formed by the uplifting of mud that is formed by thawing of the below-ground permafrost.

Cryogenic

A term used to describe the material state of being at very low temperatures. In biology, the term relates to organisms requiring low temperatures or the effects of low temperatures on organisms.

Brine veins

(Also known as liquid veins). Lines of liquid water that have high salt content within ice; they can transport soluble and insoluble particles under otherwise freezing conditions.

Acetoclastic methanogens

Archaea that produce methane using acetate as a carbon source; they are responsible for approximately two-thirds of the biogenic methane that is produced annually on Earth.

Hydrogenotrophic methanogens

Archaea that produce methane using H2, CO2 and sometimes formate as a carbon source.

Compatible solutes

(Also known as osmolytes). Small molecules that accumulate in cells to balance the osmotic difference between the inside of the cell and the surroundings of the cell; they help organisms to survive extreme osmotic stress and/or freezing conditions.

DEAD-box helicases

A family of proteins that are involved in the unwinding of RNA. RNA molecules can be mostly single stranded or can adopt specific tertiary structures and are dependent on proteins such as helicases to ensure their correct folding. DEAD-box helicases are also involved in nuclear transcription, pre-mRNA splicing, ribosome biogenesis, nucleocytoplasmic transport, translation, RNA decay and organellar gene expression.

Metagenomics

Sequencing of total community DNA, thus accessing all genes in the composite genomes of organisms (such as bacteria, archaea, eukarya and viruses) in a given sample, including phylogenetic and protein-coding genes.

Methanotrophs

Aerobic bacteria or anaerobic archaea that are able to metabolize methane (and in some cases other C1 compounds) as a source of carbon and energy.

Greenhouse gas

A gas in the atmosphere that can absorb and emit radiation within the thermal infrared range. The primary greenhouse gases in the atmosphere of the Earth are carbon dioxide, methane, nitrous oxide, water vapour and ozone.

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Jansson, J., Taş, N. The microbial ecology of permafrost. Nat Rev Microbiol 12, 414–425 (2014). https://doi.org/10.1038/nrmicro3262

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