Functional and Evolutionary Characterization of a Gene Transfer Agent’s Multilocus “Genome”

Abstract

Gene transfer agents (GTAs) are phage-like particles that can package and transfer a random piece of the producing cell’s genome, but are unable to transfer all the genes required for their own production. As such, GTAs represent an evolutionary conundrum: are they selfish genetic elements propagating through an unknown mechanism, defective viruses, or viral structures “repurposed” by cells for gene exchange, as their name implies? In Rhodobacter capsulatus, production of the R. capsulatus GTA (RcGTA) particles is associated with a cluster of genes resembling a small prophage. Utilizing transcriptomic, genetic and biochemical approaches, we report that the RcGTA “genome” consists of at least 24 genes distributed across five distinct loci. We demonstrate that, of these additional loci, two are involved in cell recognition and binding and one in the production and maturation of RcGTA particles. The five RcGTA “genome” loci are widespread within Rhodobacterales, but not all loci have the same evolutionary histories. Specifically, two of the loci have been subject to frequent, probably virus-mediated, gene transfer events. We argue that it is unlikely that RcGTA is a selfish genetic element. Instead, our findings are compatible with the scenario that RcGTA is a virus-derived element maintained by the producing organism due to a selective advantage of within-population gene exchange. The modularity of the RcGTA “genome” is presumably a result of selection on the host organism to retain GTA functionality.

Gene Transfer Agent Promotes Evolvability within the Fittest Subpopulation of a Bacterial Pathogen

“…Our study indicates that despite a distinct origin, the later steps of DNA uptake and integration into recipient cells seem conserved between BaGTA and RcGTA (Brimacombe et al., 2014, Brimacombe et al., 2015), suggesting a shared uptake mechanism between all GTA systems. This also supports the emerging view that GTA-mediated DNA transfer may generally be considered as a form of transformation rather than transduction or conjugation (Redfield, 2001, Brimacombe et al., 2015, Takeuchi et al., 2014, Hynes et al., 2016). …”

“…This is in contrast to bacteriophages, which largely promote exchange of phage-specific genes and are therefore self-transmissible. In this respect, GTAs can be considered as a form of “domesticated” prophage—that is, ancestrally derived from a bacteriophage genome but altered by the host to confer an adaptive benefit—and thus represent one of many phage-derived adaptive functions observed in bacterial genomes (Bobay et al., 2014, Hynes et al., 2016). It is, however, unclear how maintenance of a system that can induce the lysis of individual cells may still be beneficial to the entire population.

Figure 1Chromosomal Marker Exchanges during B. henselae Co-culture(A) Schematic model for BaGTA-mediated genetic exchange in Bartonella .

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Bacterial Diversification in the Light of the Interactions with Phages: The Genetic Symbionts and Their Role in Ecological Speciation

“…Another example of phage genes being repurposed with a more mutualistic role are tailocins, in which tail subunits from a phage are used in bacterial warfare (Ghequire and De Mot, 2015). Similar to GTAs, tailocins have evolved independently in several microbial groups, and in both GTAs and tailocins the organization of genes is highly similar to the organization in phage genomes, and genes are recognizably viral in origin (Ghequire and De Mot, 2015;Hynes et al, 2016). The fate of any gene lies in its replicative potential.…”

Bartonellagene transfer agent: Evolution, function, and proposed role in host adaptation

“…A recent analysis of RcGTA homologues supports its proposed phage origin and estimates that the chromosomal acquisition of this DNA transfer machinery within a subclade of the α‐proteobacteria occurred more than 500 million years ago (Shakya et al, ). RcGTAs harbour the clear signature of vertical transmission, although their evolution and spread has been further shaped by HGT (Hynes et al, ; Shakya et al, ). Interestingly, no homologues of RcGTA genes can be found in any representative of the genus Bartonella .…”

“…RcGTAs harbour the clear signature of vertical transmission, although their evolution and spread has been further shaped by HGT (Hynes et al, 2016;Shakya et al, 2017). Interestingly, no homologues of RcGTA genes can be found in any representative of the genus Bartonella.…”