title: 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.
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Alexander P
authors.initials: AP
authors.lastname: Hynes
authors.affiliation: Department of Biological Sciences, Dartmouth College.
authors.forename: Migun
authors.initials: M
authors.lastname: Shakya
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Ryan G
authors.initials: RG
authors.lastname: Mercer
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Marc P
authors.initials: MP
authors.lastname: Grüll
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Luke
authors.initials: L
authors.lastname: Bown
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Fraser
authors.initials: F
authors.lastname: Davidson
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Ekaterina
authors.initials: E
authors.lastname: Steffen
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Heidi
authors.initials: H
authors.lastname: Matchem
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Mandy E
authors.initials: ME
authors.lastname: Peach
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Tim
authors.initials: T
authors.lastname: Berger
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada.
authors.forename: Katherine
authors.initials: K
authors.lastname: Grebe
authors.affiliation: Department of Biological Sciences, Dartmouth College Department of Computer Science, Dartmouth College olga.zhaxybayeva@dartmouth.edu aslang@mun.ca.
authors.forename: Olga
authors.initials: O
authors.lastname: Zhaxybayeva
authors.affiliation: Department of Biology, Memorial University of Newfoundland, St John's, NL, Canada olga.zhaxybayeva@dartmouth.edu aslang@mun.ca.
authors.forename: Andrew S
authors.initials: AS
authors.lastname: Lang
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics; D001435:Bacteriophages / Q000235:genetics; D005075:Biological Evolution; D015964:Gene Expression Regulation, Bacterial; D022761:Gene Transfer, Horizontal / Q000235:genetics; D039002:Prophages / Q000235:genetics; D016354:Rhodobacter capsulatus / Q000235:genetics*
chemical_list: D001426:Bacterial Proteins
keywords: RcGTA; Rhodobacter.; exaptation; gene exchange; prophage; virus