‘Ménage à trois’: a selfish genetic element uses a virus to propagate within Thermotogales

Abstract

Prokaryotic viruses play a major role in the microbial ecology and evolution. However, the virosphere associated with deep-sea hydrothermal ecosystems remains largely unexplored. Numerous instances of lateral gene transfer have contributed to the complex and incongruent evolutionary history of Thermotogales, an order well represented in deep-sea hydrothermal vents. The presence of clustered regularly interspaced short palindromic repeats (CRISPR) loci has been reported in all Thermotogales genomes, suggesting that these bacteria have been exposed to viral infections that could have mediated gene exchange. In this study, we isolated and characterized the first virus infecting bacteria from the order Thermotogales, Marinitoga piezophila virus 1 (MPV1). The host, Marinitoga piezophila is a thermophilic, anaerobic and piezophilic bacterium isolated from a deep-sea hydrothermal chimney. MPV1 is a temperate Siphoviridae-like virus with a 43.7 kb genome. Surprisingly, we found that MPV1 virions carry not only the viral DNA but preferentially package a plasmid of 13.3 kb (pMP1) also carried by M. piezophila. This 'ménage à trois' highlights potential relevance of selfish genetic elements in facilitating lateral gene transfer in the deep-sea biosphere.

Two viruses, MCV1 and MCV2, which infect Marinitoga bacteria isolated from deep‐sea hydrothermal vents: functional and genomic analysis

“…In these three viral genomes the lysogeny modules appeared relatively more variable. Several hypothetical proteins are found in all three genomes, suggesting that these proteins probably provide important functions for these viruses (Lossouarn et al ., , Supporting Information Tables S2 and S3).…”

“…Four of these, BVW1, GVE1, GVE2 and D6E, are virulent (i.e., they replicate through a lytic cycle) and infect thermophilic and heterotrophic bacteria belonging to the Bacillus and Geobacillus genera (Liu et al ., ; Liu and Zhang, ; Wang and Zhang, ). The other two are temperate siphoviruses (i.e., they replicate through a lysogenic cycle), NrS1 infects a thermophilic Epsilonproteobacterium belonging to the Nitratiruptor genus (Yoshida‐Takashima et al ., ) and MPV1 infects Marinitoga piezophila , a bacterium from the Petrotogales order and Thermotogae phylum (Lossouarn et al ., ).…”

“…Similarly to many thermophilic microorganisms, clustered regularly interspaced short palindromic repeats (CRISPRs) are present in numerous Thermotogae genome sequences (Zhaxybayeva et al, 2009;Nesbø et al, 2015;Haverkamp et al, unpublished), suggesting that they were exposed to viral infections during the course of their evolutionary history. However, only one virus has been described in this phylum, MPV1 carried by Marinitoga piezophila KA3 (Alain et al, 2002;Lossouarn et al, 2015b). MPV1 is a temperate siphovirus with a genome of 43.7 kb matching the provirus integrated in M. piezophila KA3 chromosome (Lucas et al, 2012).…”

“…This host carries a second mobile genetic element, a plasmid of 13.3 kb (referred as pMP1). Remarkably, pMP1 uses the MPV1 viral capsid to propagate, highlighting a complex evolutionary relationship between a bacterial host, an extrachromosomal element and a virus (Lossouarn et al, 2015b).…”

Draft Genome Sequences of Two Marinitoga camini Isolates Producing Bacterioviruses

“…This site is located at 1700 m of depth in the Mid-Atlantic Ridge (8). Strains DV1197 and DV1155 grow optimally at 60°C and 65°C, respectively, at atmospheric pressure in a modified Ravot medium (9) with elemental sulfur instead of cysteine.…”