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Rebooting the genome: The role of negative feedback in horizontal gene transfer.

ABSTRACT: Horizontal Gene Transfer (HGT) is one of the key mechanisms driving bacterial evolution. Conjugative plasmids are fundamental vehicles for HGT in bacteria, playing an essential role in the spread of antibiotic resistances. Although the classical view has stressed the instrumental role of these mobile genetic elements in the dissemination of antibiotic resistance genes, plasmids contain a rich physiology devoted to horizontal and vertical reproduction. This particular lifestyle imposes specific constrains and trade-offs on plasmid physiology, and plasmids have evolved dedicated circuits to balance the opposing demands of vertical and horizontal reproduction. Recent studies on the transcriptional networks of IncW plasmids and other incompatibility groups have unveiled common architectures in the regulatory networks of different plasmid groups. Comparative studies show that negative feedback loops (NFLs) with strong gains are preferred, opening the question of a possible convergent evolution dictated by certain adaptive properties of this particular network motif. System analysis of NFLs with strong feedback gains indicate that this architecture exhibits transient overshooting after horizontal gene transfer. Since plasmid burden is dependent on the expression of plasmid functions, transcriptional overshooting results in a transient increase of the burden immediately after conjugation. We discuss the possible implications of this phenomenon on plasmid propagation, and the regulatory networks that plasmids have evolved to counteract the detrimental side effects of transient overshooting.

SUBMITTER: Fernandez-Lopez R

PROVIDER: S-EPMC4588214 | biostudies-other | 2014 Nov-Dec

REPOSITORIES: biostudies-other

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Project description:BackgroundGenomes of Methanosarcina spp. are among the largest archaeal genomes. One suggested reason for that is massive horizontal gene transfer (HGT) from bacteria. Genes of bacterial origin may be involved in the central metabolism and solute transport, in particular sugar synthesis, sulfur metabolism, phosphate metabolism, DNA repair, transport of small molecules etc. Horizontally transferred (HT) genes are considered to play the key role in the ability of Methanosarcina spp. to inhabit diverse environments. At the moment, genomes of three Methanosarcina spp. have been sequenced, and while these genomes vary in length and number of protein-coding genes, they all have been shown to accumulate HT genes. However, previous estimates had been made when fewer archaeal genomes were known. Moreover, several Methanosarcinaceae genomes from other genera have been sequenced recently. Here, we revise the census of genes of bacterial origin in Methanosarcinaceae.ResultsAbout 5% of Methanosarcina genes have been shown to be horizontally transferred from various bacterial groups to the last common ancestor either of Methanosarcinaceae, or Methanosarcina, or later in the evolution. Simulation of the composition of the NCBI protein non-redundant database for different years demonstrates that the estimates of the HGT rate have decreased drastically since 2002, the year of publication of the first Methanosarcina genome. The phylogenetic distribution of HT gene donors is non-uniform. Most HT genes were transferred from Firmicutes and Proteobacteria, while no HGT events from Actinobacteria to the common ancestor of Methanosarcinaceae were found. About 50% of HT genes are involved in metabolism. Horizontal transfer of transcription factors is not common, while 46% of horizontally transferred genes have demonstrated differential expression in a variety of conditions. HGT of complete operons is relatively infrequent and half of HT genes do not belong to operons.ConclusionsWhile genes of bacterial origin are still more frequent in Methanosarcinaceae than in other Archaea, most HGT events described earlier as Methanosarcina-specific seem to have occurred before the divergence of Methanosarcinaceae. Genes horizontally transferred from bacteria to archaea neither tend to be transferred with their regulators, nor in long operons.

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Rebooting the genome: The role of negative feedback in horizontal gene transfer.

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