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Mechanisms of gene flow in archaea

Key Points

  • Horizontal gene transfer (HGT) is essential for genome evolution across the tree of life and has an important role in archaeal speciation, adaptation, and maintenance of diversity.

  • Many of the horizontally acquired genes in archaea are involved in metabolism and cell envelope biogenesis and therefore likely provided a selective advantage for adaptation to new environments.

  • The transfer of DNA can also function in DNA repair by providing an intact template for homologous recombination, as has been shown for Sulfolobus spp.

  • Classic bacterial DNA transfer mechanisms, such as transformation, conjugation and transduction, have been identified in certain archaeal species. In addition, DNA exchange through vesicles, through cell fusion and by the recently discovered archaea-specific crenarchaeal exchange of DNA (Ced) system has been observed.

  • Several barriers prevent the transfer and incorporation of foreign DNA in archaeal species; these include physical environmental barriers, the surface layer (S-layer), CRISPR–Cas systems, restriction–modification systems and toxin–antitoxin systems.

  • Newly identified and sequenced species will enable us to uncover more HGT events among and between archaea, bacteria and eukaryotes.

  • With an increasing number of genetically tractable archaeal species, we will be able to elucidate the processes that underlie gene flow in archaea.

Abstract

Archaea are diverse, ecologically important, single-celled microorganisms. They have unique functions and features, such as methanogenesis and the composition of their cell envelope, although many characteristics are shared with the other domains of life, either through ancestry or through promiscuous horizontal gene transfer. The exchange of genetic material is a major driving force for genome evolution across the tree of life and has a role in archaeal speciation, adaptation and maintenance of diversity. In this Review, we discuss our current knowledge of archaeal mechanisms of DNA transfer and highlight the role of gene transfer in archaeal evolution.

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Figure 1: DNA transfer mechanisms in archaea.
Figure 2: DNA transfer in Sulfolobales.
Figure 3: Barriers to HGT.

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Acknowledgements

R.J.W. and D.J.K. acknowledge funding support from the US National Science Foundaion (NSF; grant DEB #1355171) and NASA Exobiology and Evolutionary Biology (grant NNX09AM92G). A.W., M.v.W. and J.H. were supported by a European Research Council (ERC) starting grant (grant ARCHAELLUM, 311523). J.H. received further support from the CRC746 (DFG).

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Glossary

TACK superphylum

A recently proposed superphylum that comprises the Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota phyla.

Asgard superphylum

A recently described superphylum that includes the proposed Lokiarchaeota, Odinarchaeota, Thorarchaeota and Heimdallarchaeota phyla. Asgardarchaeota encode many proteins that were previously suspected to be specific for eukaryotes.

DPANN superphylum

A proposed monophyletic and deep-branching group of mainly hyperthermophilic archaea that includes the Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota and Nanohaloarchaeota phyla.

Heterotrophs

Organisms that produce complex organic compounds from organic carbon.

Autotrophs

Organisms that produce complex organic compounds from inorganic material using light energy (photosynthesis) or chemical energy (chemosynthesis).

Mesophilic archaea

Archaea that grow at temperatures ranging from 20–45 °C.

Type IV secretion system

(T4SS). A secretion system found in many bacteria and some archaea that is involved in the secretion of proteins, DNA and protein–DNA complexes into target cells.

Hyperthermophile

An organism that can thrive at temperatures around 80 °C or higher.

Nanopods

Surface structures that project membrane vesicles from the cell. Nanopods have been found in bacteria and members of the Euryarchaeota.

Proviruses

Viral DNAs that are integrated into the genome of its host.

Episomes

Fragments of DNA that exist independently of the chromosome. Examples of episomes include insertion elements, transposons, plasmids and viruses.

Temperate viruses

Viruses that can integrate into the chromosome or lyse the cell following infection or induction.

Gene transfer agents

A bacteriophage-like element in bacteria that mediates horizontal gene transfer by transducing random host DNA into a recipient cell.

CRISPR–Cas

An adaptive immune system in bacteria and archaea that enables the acquisition of resistance to foreign genetic elements, such as plasmids and viruses.

Partitioning system

A system that ensures the correct segregation of chromosomal DNA or plasmids into the daughter cells of a dividing bacterial cell.

Hetero-diploid

Cells that have two different homologous chromosomes.

Type IV pilus

A surface appendage found in many bacteria and archaea. Type IV pili are involved in motility and attachment to surfaces and other cells.

Polytopic membrane protein

A protein that has multiple transmembrane domains.

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Wagner, A., Whitaker, R., Krause, D. et al. Mechanisms of gene flow in archaea. Nat Rev Microbiol 15, 492–501 (2017). https://doi.org/10.1038/nrmicro.2017.41

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