Molecular piracy in deep-sea hydrothermal vent: phage-plasmid interactions revealed by phage-FISH in Marinitoga piezophila.

Abstract

Prokaryotes and mobile genetic elements (MGEs, such as viruses and plasmids) interact extensively, leading to horizontal gene transfer (HGT) and consequent microbial evolution and diversity. However, our knowledge of the interactions between MGEs in deep-sea hydrothermal ecosystems is limited. In this study, we adapted a phage-fluorescence in situ hybridization (phage-FISH) approach to visualize and quantify the dynamics of phage-plasmid interactions in an anaerobic, thermophilic deep-sea bacterium, Marinitoga piezophila. Notably, our results revealed that plasmid signals were detected in viral particles released from lysed cells, indicating that mitomycin C not only induced plasmid replication but also its packaging into phage particles. Further analysis of the DNA content in purified virions showed that the phage capsids incorporated plasmid DNA even without induction, and the majority of capsids (up to 70%) preferentially packaged plasmid DNA rather than viral DNA after induction. Therefore, this study provided direct evidence of molecular piracy in the deep-sea hydrothermal ecosystem, highlighting the important roles of selfish MGEs in virus-host interactions and HGT in extreme marine environments.

Importance: Deep-sea hydrothermal vents are hotspots for microbes. Several studies revealed that virus-mediated horizontal gene transfer (HGT) in deep-sea hydrothermal vent ecosystems may be crucial to the survival and stability of prokaryotes in these extreme environments. However, little is known about the interaction between viruses and other mobile genetic elements (MGEs, such as plasmids), and how their interactions influence virus-mediated HGT in these ecosystems. In this study, we adapted a phage-fluorescence in situ hybridization approach to directly monitor the dynamics of phage-plasmid-host interactions at the single-cell level in the Marinitoga piezophila model. Interestingly, our results indicate that plasmid DNA could not only be induced by mitomycin C to a great extent but also hijacked viral assembly machinery to facilitate its propagation and spread. Therefore, the data presented here imply that the interaction between the viruses and other MGEs could play profound roles in virus-host interaction and virus-mediated HGT in the deep-sea hydrothermal ecosystem.