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  • Review Article
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Gene transfer agents: phage-like elements of genetic exchange

Key Points

  • Gene transfer agents (GTAs) are phage-like entities that contain a random piece of the genome of the producing cell. The amount of DNA that a GTA contains is insufficient to encode the protein components of the particle itself. Instead, structural GTA genes are encoded within the genome of the producing cell.

  • All known GTAs have tailed-phage structures, which presumably are released into the environment by lysis of the producing cell. Released GTA particles can transfer DNA from the producing cell to a recipient cell. GTAs are thought to bind to recipient cells through specific tail–receptor interactions, but no receptors have been identified to date.

  • Four genetically unrelated GTAs have been identified to date: RcGTA in the alphaproteobacterium Rhodobacter capsulatus, Dd1 in the deltaproteobacterium Desulfovibrio desulfuricans, VSH-1 (virus of Serpulina hyodysenteriae) in the spirochaete Brachyspira hyodysenteriae and VTA (voltae transfer agent) in the archaeon Methanococcus voltae. Two of these entities, RcGTA and Dd1, have been characterized in detail, and there are some details available for VSH-1 and VTA.

  • The known GTAs show structural similarity to siphoviruses or podoviruses. There are several possible evolutionary scenarios that would explain the connections between GTAs and phages, as well as some evidence suggesting that the four known GTAs evolved independently.

  • There are various potential functions for GTA-mediated gene transfer. One suggestion is that GTAs are public goods which provide a means of altruistic cooperation between related microorganisms.

Abstract

Horizontal gene transfer is important in the evolution of bacterial and archaeal genomes. An interesting genetic exchange process is carried out by diverse phage-like gene transfer agents (GTAs) that are found in a wide range of prokaryotes. Although GTAs resemble phages, they lack the hallmark capabilities that define typical phages, and they package random pieces of the producing cell's genome. In this Review, we discuss the defining characteristics of the GTAs that have been identified to date, along with potential functions for these agents and the possible evolutionary forces that act on the genes involved in their production.

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Figure 1: Comparison of gene transfer agent and transducing phage production.
Figure 2: Electron micrographs of gene transfer agent particles.
Figure 3: Gene transfer agent-encoding gene clusters.
Figure 4: Distribution of gene transfer agent genes in alphaproteobacteria and spirochaetes.
Figure 5: Evidence of purifying selection in selected gene transfer agent genes in the Rhodobacterales order of the class Alphaproteobacteria.

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Acknowledgements

This work is supported by funding from the National Science and Engineering Research Council of Canada and the Newfoundland and Labrador Research and Development Corporation to A.S.L.; by West Virginia University (Morgantown, USA) startup funds to O.Z.; and by the Canadian Institutes of Health Research to J.T.B. The authors thank R. T. Papke and J. P. Gogarten for stimulating discussions, and F. Eiserling, B. Marrs, T. Stanton and J. Wall for permission to use their electron microscopy images in figure 2. The authors regret their inability to cite all relevant research literature owing to space constraints.

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Lang, A., Zhaxybayeva, O. & Beatty, J. Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol 10, 472–482 (2012). https://doi.org/10.1038/nrmicro2802

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