Abstract
SummaryAlthough plasmids play an important role in biological evolution, the number of plasmid families well‐characterized in terms of geographical distribution and evolution remains limited, especially in archaea. Here, we describe the first systematic study of an archaeal plasmid family, the pT26‐2 plasmid family. The in‐depth analysis of the distribution, biogeography and host–plasmid co‐evolution patterns of 26 integrated and 3 extrachromosomal plasmids of this plasmid family shows that they are widespread in Thermococcales and Methanococcales isolated from around the globe but are restricted to these two orders. All members of the family share seven core genes but employ different integration and replication strategies. Phylogenetic analysis of the core genes and CRISPR spacer distribution suggests that plasmids of the pT26‐2 family evolved with their hosts independently in Thermococcales and Methanococcales, despite these hosts exhibiting similar geographic distribution. Remarkably, core genes are conserved even in integrated plasmids that have lost replication genes and/or replication origins suggesting that they may be beneficial for their hosts. We hypothesize that the core proteins encode for a novel type of DNA/protein transfer mechanism, explaining the widespread oceanic distribution of the pT26‐2 plasmid family.
Highlights
Mobile genetic elements (MGEs) are a crucial component of the living world, being the major vehicles for horizontal gene transfer (HGT; Koonin and Wolf, 2008), agents of genomic recombination (Cossu et al, 2017) and cradles of novel genes (Keller et al, 2009; Forterre and Gaïa, 2016; Legendre et al, 2018)
Whereas archaea are much more closely related to eukaryotes than to bacteria in terms of fundamental molecular mechanisms, the set of MGEs infecting archaea and bacteria are strikingly similar and very different from those present in eukaryotes (Forterre, 2013; Forterre et al, 2014). It is unclear if the observed resemblance between the archaeal and bacterial mobilomes is a result of convergence due to the comparable chromosome structure and organization of archaeal and bacterial cells, or if it reflects widespread distribution of these MGEs by HGT between these two domains or perhaps inheritance of a similar type of MGE present in the Last Universal Common Ancestor
In order to expand the diversity of plasmids of the pT26-2 family, each of the seven previously identified core genes (Soler et al, 2010) were used as query sequences to identify homologues in complete or partial archaeal, bacterial or eukaryotic genomes
Summary
Mobile genetic elements (MGEs) are a crucial component of the living world, being the major vehicles for horizontal gene transfer (HGT; Koonin and Wolf, 2008), agents of genomic recombination (Cossu et al, 2017) and cradles of novel genes (Keller et al, 2009; Forterre and Gaïa, 2016; Legendre et al, 2018). Whereas archaea are much more closely related to eukaryotes than to bacteria in terms of fundamental molecular mechanisms (replication, transcription and translation), the set of MGEs (mobilome) infecting archaea and bacteria are strikingly similar and very different from those present in eukaryotes (Forterre, 2013; Forterre et al, 2014). It is unclear if the observed resemblance between the archaeal and bacterial mobilomes is a result of convergence due to the comparable chromosome structure and organization of archaeal and bacterial cells, or if it reflects widespread distribution of these MGEs by HGT between these two domains or perhaps inheritance of a similar type of MGE present in the Last Universal Common Ancestor. Other MGEs have been detected in the course of genome sequencing projects, either as extrachromosomal or integrated plasmids (Fukui et al, 2005; Zivanovic et al, 2009; Vannier et al, 2011)
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