Abstract
Horizontal gene transfer (HGT) contributes greatly to the plasticity and evolution of prokaryotic and eukaryotic genomes. The main carriers of foreign DNA in HGT are mobile genetic elements (MGEs) that have extremely diverse genetic structures and properties. Various strategies are used for the maintenance and spread of MGEs, including (i) vegetative replication, (ii) transposition (and other types of recombination), and (iii) conjugal transfer. In many MGEs, all of these processes are dependent on rolling-circle replication (RCR). RCR is one of the most well characterized models of DNA replication. Although many studies have focused on describing its mechanism, the role of replication initiator proteins has only recently been subject to in-depth analysis, which indicates their involvement in multiple biological process associated with RCR. In this review, we present a general overview of RCR and its impact in HGT. We focus on the molecular characteristics of RCR initiator proteins belonging to the HUH and Rep_trans protein families. Despite analogous mechanisms of action these are distinct groups of proteins with different catalytic domain structures. This is the first review describing the multifunctional character of various types of RCR initiator proteins, including the latest discoveries in the field. Recent reports provide evidence that (i) proteins initiating vegetative replication (Rep) or mobilization for conjugal transfer (Mob) may also have integrase (Int) activity, (ii) some Mob proteins are capable of initiating vegetative replication (Rep activity), and (iii) some Rep proteins can act like Mob proteins to mobilize plasmid DNA for conjugal transfer. These findings have significant consequences for our understanding of the role of RCR, not only in DNA metabolism but also in the biology of many MGEs.
Highlights
Rolling-circle replication (RCR) was first described nearly half a century ago following analysis of the replication of Escherichia coli bacteriophage X174 (Gilbert and Dressler, 1968; Dressler, 1970)
Rolling-circle replication is involved in various processes conducted by genetic elements, including (i) replication of their autonomous forms, (ii) conjugal transfer, (iii) transposition (TEs), and (iv) recombination
Such replication is mediated by helitrons and ISCRs as well as by some conjugative plasmids, which temporarily integrate into the host chromosome
Summary
Rolling-circle replication (RCR) was first described nearly half a century ago following analysis of the replication of Escherichia coli bacteriophage X174 (Gilbert and Dressler, 1968; Dressler, 1970). It is thought that some transposable elements, such as bacterial IS91-like insertion sequences and eukaryotic helitrons, use RCR to replicate in host genomes (Mendiola et al, 1994; Thomas and Pritham, 2015). According to their biological roles, RCR initiator proteins are divided into three groups: Rep proteins (vegetative replication), Mob proteins (mobilization for conjugal transfer) and Tnp proteins (transposition). A number of reports concerning RCR replication have recently been published (e.g., Wang et al, 2013; Boer et al, 2016; Carr et al, 2016; Wright and Grossman, 2016) These have revealed new facts about RCR and especially the role of the replication initiator proteins. Different RCR variants are compared, and features and functions of selected multifunctional RCR initiator proteins encoded by mobile genetic elements (MGEs) are described
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