Abstract:The replication protein of the archaeal plasmid pRN1 is a multifunctional enzyme which appears to carry out several steps at the plasmid replication initiation. We recently determined the structure of the minimal primase domain of the replication protein and found out that the primase domain consists of a catalytic primase/polymerase domain and an accessory helix-bundle domain. Structure-guided mutagenesis allowed us to identify amino acids which are important for template binding, dinucleotide formation and a… Show more
“…The latter contains the N-terminal primpol domain homologous to the small subunit of archaeo-eukaryotic primases and the C-terminal superfamily 3 helicase domain. The two domains, either separately or in combination, are frequently found in various plasmids and viruses from all three cellular domains ( Iyer et al 2005 ; Lipps 2011 ; Krupovic et al 2013 ; Gill et al 2014 ). F ig .…”
Casposons are a superfamily of putative self-synthesizing transposable elements that are predicted to employ a homolog of Cas1 protein as a recombinase and could have contributed to the origin of the CRISPR-Cas adaptive immunity systems in archaea and bacteria. Casposons remain uncharacterized experimentally, except for the recent demonstration of the integrase activity of the Cas1 homolog, and given their relative rarity in archaea and bacteria, original comparative genomic analysis has not provided direct indications of their mobility. Here, we report evidence of casposon mobility obtained by comparison of the genomes of 62 strains of the archaeon Methanosarcina mazei. In these genomes, casposons are variably inserted in three distinct sites indicative of multiple, recent gains, and losses. Some casposons are inserted into other mobile genetic elements that might provide vehicles for horizontal transfer of the casposons. Additionally, many M. mazei genomes contain previously undetected solo terminal inverted repeats that apparently are derived from casposons and could resemble intermediates in CRISPR evolution. We further demonstrate the sequence specificity of casposon insertion and note clear parallels with the adaptation mechanism of CRISPR-Cas. Finally, besides identifying additional representatives in each of the three originally defined families, we describe a new, fourth, family of casposons.
“…The latter contains the N-terminal primpol domain homologous to the small subunit of archaeo-eukaryotic primases and the C-terminal superfamily 3 helicase domain. The two domains, either separately or in combination, are frequently found in various plasmids and viruses from all three cellular domains ( Iyer et al 2005 ; Lipps 2011 ; Krupovic et al 2013 ; Gill et al 2014 ). F ig .…”
Casposons are a superfamily of putative self-synthesizing transposable elements that are predicted to employ a homolog of Cas1 protein as a recombinase and could have contributed to the origin of the CRISPR-Cas adaptive immunity systems in archaea and bacteria. Casposons remain uncharacterized experimentally, except for the recent demonstration of the integrase activity of the Cas1 homolog, and given their relative rarity in archaea and bacteria, original comparative genomic analysis has not provided direct indications of their mobility. Here, we report evidence of casposon mobility obtained by comparison of the genomes of 62 strains of the archaeon Methanosarcina mazei. In these genomes, casposons are variably inserted in three distinct sites indicative of multiple, recent gains, and losses. Some casposons are inserted into other mobile genetic elements that might provide vehicles for horizontal transfer of the casposons. Additionally, many M. mazei genomes contain previously undetected solo terminal inverted repeats that apparently are derived from casposons and could resemble intermediates in CRISPR evolution. We further demonstrate the sequence specificity of casposon insertion and note clear parallels with the adaptation mechanism of CRISPR-Cas. Finally, besides identifying additional representatives in each of the three originally defined families, we describe a new, fourth, family of casposons.
“…Inspection of the smaller islands revealed yet uncharacterized putative elements that encode a protein (arCOG07809, e.g., Mpal_2033 from Methanosphaerula palustris ) distantly related to the primase-polymerase (prim-pol) domains of replication proteins from plasmids of Sulfolobus (Lipps 2011; Prato et al 2008) and Thermococcus (Gill et al 2014; Krupovic et al 2013) as well as certain bacterial viruses (Halgasova et al 2012). All these proteins are members of the large superfamily of archaeao-eukaryotic primases (AEP) which also includes the catalytic subunit of the archaeal and eukaryotic primases, the enzymes responsible for the initiation of DNA replication (Iyer et al 2005).…”
Section: Resultsmentioning
confidence: 99%
“…In different AEP members, the prim-pol domains possess a broad range of enzymatic activities (Gill et al 2014) and are often fused to a variety of functionally and structurally distinct domains (Iyer et al 2005). For example, in ORF904 from S. islandicus plasmid pRN1, the N-terminal prim-pol domain is followed by superfamily 3 helicase and winged helix–turn–helix (wHTH) domain (Lipps 2011; Lipps et al 2004). A similar prim-pol protein is encoded by pSSVx which is a fusellovirus satellite virus from S. islandicus that combines features of a plasmid and a virus (Arnold et al 1999; Contursi et al 2014).…”
Microbial genomes encompass a sizable fraction of poorly characterized, narrowly spread fast-evolving genes. Using sensitive methods for sequences comparison and protein structure prediction, we performed a detailed comparative analysis of clusters of such genes, which we denote “dark matter islands”, in archaeal genomes. The dark matter islands comprise up to 20 % of archaeal genomes and show remarkable heterogeneity and diversity. Nevertheless, three classes of entities are common in these genomic loci: (a) integrated viral genomes and other mobile elements; (b) defense systems, and (c) secretory and other membrane-associated systems. The dark matter islands in the genome of thermophiles and mesophiles show similar general trends of gene content, but thermophiles are substantially enriched in predicted membrane proteins whereas mesophiles have a greater proportion of recognizable mobile elements. Based on this analysis, we predict the existence of several novel groups of viruses and mobile elements, previously unnoticed variants of CRISPR-Cas immune systems, and new secretory systems that might be involved in stress response, intermicrobial conflicts and biogenesis of novel, uncharacterized membrane structures.Electronic supplementary materialThe online version of this article (doi:10.1007/s00792-014-0672-7) contains supplementary material, which is available to authorized users.
“…Viruses and plasmids encode a number of common proteins that do not have homologues in cellular proteomes. Notable examples of such proteins are initiators of rolling-circle replication, superfamily III helicases, or primase/ polymerase proteins (138,167), which are specific to viruses and plasmids and do not participate in the replication of cellular chromosomes. The origin of other mobile genetic elements (MGEs), such as transposons, integrons, and genomic islands (271), might also stem from ancient viruses (84).…”
Section: Genomic Relationship To Other Mobile Genetic Elementsmentioning
SUMMARY
Prokaryotes, bacteria and archaea, are the most abundant cellular organisms among those sharing the planet Earth with human beings (among others). However, numerous ecological studies have revealed that it is actually prokaryotic viruses that predominate on our planet and outnumber their hosts by at least an order of magnitude. An understanding of how this viral domain is organized and what are the mechanisms governing its evolution is therefore of great interest and importance. The vast majority of characterized prokaryotic viruses belong to the order Caudovirales, double-stranded DNA (dsDNA) bacteriophages with tails. Consequently, these viruses have been studied (and reviewed) extensively from both genomic and functional perspectives. However, albeit numerous, tailed phages represent only a minor fraction of the prokaryotic virus diversity. Therefore, the knowledge which has been generated for this viral system does not offer a comprehensive view of the prokaryotic virosphere. In this review, we discuss all families of bacterial and archaeal viruses that contain more than one characterized member and for which evolutionary conclusions can be attempted by use of comparative genomic analysis. We focus on the molecular mechanisms of their genome evolution as well as on the relationships between different viral groups and plasmids. It becomes clear that evolutionary mechanisms shaping the genomes of prokaryotic viruses vary between different families and depend on the type of the nucleic acid, characteristics of the virion structure, as well as the mode of the life cycle. We also point out that horizontal gene transfer is not equally prevalent in different virus families and is not uniformly unrestricted for diverse viral functions.
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