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  • Review Article
  • Published:

Cold-adapted archaea

Nature Reviews Microbiology volume 4, pages 331–343 (2006)Cite this article

Key Points

  • Most of the Earth's biosphere is cold, and psychrophilic microorganisms can be found in these permanently cold environments (≤5°C).

  • Archaea are ubiquitous microorganisms that are present in most terrestrial and aquatic environments.

  • Diverse functional roles have been established for psychrophilic archaea, and molecular analyses have established their importance in a wide variety of cold environments. These include marine environments (coastal, open-ocean and deep-sea waters, sea ice, marine-based lakes, sediment and subsurface, digestive tracts and faeces of animals, marine snow and sponges) and non-marine environments (soils including rhizosphere, landfills, farms, permafrost, glaciers and streams, alpine lakes, wetlands, freshwater sediments and anaerobic bioreactors).

  • Despite the largest proportion and greatest diversity of archaea existing in cold environments, few psychrophilic archaea have been isolated.

  • Most isolated psychrophilic archaea are methanogens, and others include a halophile, a euryarchaeon associated with bacteria and a crenarchaeon, a marine sponge symbiont.

  • Cellular mechanisms of cold adaptation have largely been derived from the model eurypsychrophilic archaeon Methanococcoides burtonii, and have included studies of protein structure and function, intracellular solutes, gene regulation, tRNA modification, membrane-lipid composition, genomics and proteomics.

  • Cold shock is physiologically relevant to non-psychrophilic archaea, and these molecular responses have begun to be characterized in hyperthermophiles.

  • Ace Lake and other lakes in the Vestfold Hills region of Antarctica are diverse, pristine systems, ideal for studying the biota and biogeochemistry of cold environments.

  • Cold-adapted archaea, and in particular methanogens, offer important insights into the search for extraterrestrial life.

Abstract

Many archaea are extremophiles. They thrive at high temperatures, at high pressure and in concentrated acidic environments. Nevertheless, the largest proportion and greatest diversity of archaea exist in cold environments. Most of the Earth's biosphere is cold, and archaea represent a significant fraction of the biomass. Although psychrophilic archaea have long been the neglected majority, the study of these microorganisms is beginning to come of age. This review casts a spotlight on the ecology, adaptation biology and unique science that is being realized from studies on cold-adapted archaea.

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Figure 1: Diversity of archaea from naturally cold environments.
Figure 2: Cellular processes that are important for cold adaptation in Methanococcoides burtonii.

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Acknowledgements

I dedicate this article to David R. Boone, who died May 27, 2005. As part of the Oregon Collection of Methanogens that he created and directed, David worked tirelessly to isolate and characterize key psychrophilic methanogens. I am deeply indebted to G. Jurgens, who generously constructed the phylogenetic tree, and to K. Sowers and G. Ferry, who provided a stimulating environment during my sabbatical. A special thanks to J. Bowman, J. Gibson, P. Franzmann, K. Kastead, J. Biddle, T. Kolesnikow, past and present members of my lab, and a broad range of colleagues who have, in effect, formed the backbone of this manuscript. This review could not be exhaustive and I regret not being able to cite all relevant literature. Research in my lab is supported by the Australian Research Council.

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  1. School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, NSW 2052, Australia

    Ricardo Cavicchioli

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DATABASES

Entrez Genome Project

Cenarchaeum symbiosum

Colwellia psychrerythraea

Escherichia coli

Halobacterium NRC-1

Haloferax volcanii

Halorubrum lacusprofundi

Listeria monocytogenes

Methanocaldococcus jannaschii

Methanococcoides burtonii

Methanogenium frigidum

Methanopyrus kandleri

Pyrococcus furiosus

Sphingopyxis alaskensis

Sulfolobus acidocaldarius

FURTHER INFORMATION

Ricardo Cavicchioli's homepage

Australian Antarctic Division

ArchaeaWeb

DOE Joint Genome Institute (JGI)

Draft genomes: sequence and analyses

Methanococcoides burtonii at the JGI

Why Sequence Six Archaea? (at the JGI)

The J. Craig Venter Institute

The Gordon and Betty Moore Foundation

Microbial Genome Sequencing Project at the Gordon and Betty Moore Foundation

Glossary

Psychrophile

An organism that grows in a cold environment.

Shelford's law of tolerance

A concept of ecological tolerance in which each ecological factor to which an organism responds has maximum and minimum limiting effects between which lies a range that it can tolerate.

Heterotroph

An organism that uses organic compounds as nutrients to produce energy for growth.

Crenarchaeota

One of the four kingdoms of the Archaea, phylogenetically distinct from the Euryarchaeota, Korarchaeota and Nanoarchaeota.

Rhizosphere

The soil zone that surrounds, and is effected by, the roots of plants.

Nitrifiers

Organisms that convert ammonia into a more oxidized form such as nitrate or nitrite.

Meromictic

Meromictic lakes contain a bottom layer of water that does not mix with the upper layer of water. The upper mixed layer (mixolimnion) is typically separated from the lower stagnant anoxic layer (monimolimnion) by a steep density gradient (pycnocline).

Methylotrophic methanogen

Compared to hydrogenotrophic methanogens that use H2 plus CO2 (or formate), methylotrophs use simple C1 compounds such as methanol, methylamines and methylthiols to grow and produce methane.

Chlorophyte

Photosynthetic alga that is a member of the Chlorophyta phylum of eukaryal protists.

Chemolithoautotroph

An organism that obtains energy from inorganic compounds and carbon from CO2.

Mesophile

An organism that is typically isolated from a moderate environment (∼20?45°C) and that can grow effectively in its natural environment.

Elongation factor 2

(EF2). GTPase that interacts with the ribosome and has an essential role in the elongation step of translation during protein synthesis.

Principle components analysis

A statistical method that can be applied to a multivariate data set to reduce the complexity of the data and to determine whether there are underlying trends that explain the observed variation.

Molecular chaperone

A protein that assists protein folding by preventing peptides emerging from the ribosome from becoming misfolded, or that might refold misfolded proteins (for example, during cellular stress); includes the chaperonin protein-folding machine.

Peptidyl-prolyl cis/trans isomerase

(PPIase). Enzyme that increases the rate at which proteins can fold by catalysing the otherwise rate-limiting cis/trans isomerization of proline imide bonds in polypeptides.

Accretion ice

Ice that has formed after lake water freezes when it comes into contact with colder glacial ice that is above it.

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Cavicchioli, R. Cold-adapted archaea. Nat Rev Microbiol 4, 331–343 (2006). https://doi.org/10.1038/nrmicro1390

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