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Adaptations to energy stress dictate the ecology and evolution of the Archaea

Abstract

The three domains of life on Earth include the two prokaryotic groups, Archaea and Bacteria. The Archaea are distinguished from Bacteriabased on phylogenetic and biochemical differences, but currently there is no unifying ecological principle to differentiate these groups. The ecology of the Archaea is reviewed here in terms of cellular bioenergetics. Adaptation to chronic energy stress is hypothesized to be the crucial factor that distinguishes the Archaea from Bacteria. The biochemical mechanisms that enable archaea to cope with chronic energy stress include low-permeability membranes and specific catabolic pathways. Based on the ecological unity and biochemical adaptations among archaea, I propose the hypothesis that chronic energy stress is the primary selective pressure governing the evolution of the Archaea.

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Figure 1: Cellular energy budgets.
Figure 2: Temperature and pH requirements for growth distinguish thermophilic bacteria and archaea.
Figure 3: Membranes of the Archaea and Bacteria.
Figure 4: Adaptations of methanogens to energy stress.

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Acknowledgements

R.C. Valentine assisted in developing ideas about membrane function. C. Francis, J. Perona, M. Facciotti and C. Schleper provided useful comments on the manuscript. Support from the US National Science Foundation contributed to the formulation of this work.

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List of prokaryotic names with standing in nomenclature

Glossary

Archaea

One of the three primary domains of life, inclusive of all organisms in the domain.

Archaeon

(archaea). An organism (organisms) belonging to the domain Archaea.

bacteria

A population or group of organisms belonging to the domain Bacteria.

Bacteria

One of the three primary domains of life, inclusive of all organisms within the domain.

Biological energy quantum

(BEQ). Finite minimum level of energy that an organism can conserve from catabolism.

Chemiosmotic

The use of an ion gradient across a membrane to generate ATP.

Clade

A hypothesis of evolutionary relatedness in which a group of organisms share a single common ancestor. In the context of microbial ecology this term is often used to indicate a group of organisms that have been shown to be monophyletic by comparative analysis of 16S rRNA or other conserved gene sequences.

Chronic energy stress

Condition in which cells are consistently faced with an insufficient supply of cellular energy. The stresses considered here to comprise chronic energy stress include the high rates of futile ion cycling driven by extreme temperature, acidity or salinity, as well as low rates of cellular energy generation due to limited substrate availability and/or unfavourable thermodynamic conditions.

Environmental exclusivity

The concept that some archaea are adapted to thrive in conditions that are inhospitable to bacteria.

Extremely halophilic

An organism that grows best in media that contains 2.5–5.2 M salt.

Maintenance energy

(ME). Minimum intake flux of energy (power) that is required to maintain molecular and cellular integrity as well as activity.

Metabolic exclusivity

The concept that dominance can be achieved by way of catabolic specialization.

Singularity of catabolism

Exclusive reliance on a single, highly specialized form of catabolism, such as methanogenesis.

Syntrophically

A syntrophic reaction is one in which two (or more) organisms interact metabolically to consume a substrate that neither can consume independently.

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Valentine, D. Adaptations to energy stress dictate the ecology and evolution of the Archaea. Nat Rev Microbiol 5, 316–323 (2007). https://doi.org/10.1038/nrmicro1619

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