As the most abundant biological entities on the planet, viruses significantly influence the overall functioning of marine ecosystems. The abundance, distribution, and biodiversity of viral communities in the upper ocean have been relatively well studied, but our understanding of viruses in the hadal biosphere remains poor. Here, we established the oceanic trench viral genome dataset (OTVGD) by analysing 19 microbial metagenomes derived from seawater and sediment samples of the Mariana, Yap, and Kermadec Trenches. The trench viral communities harbored remarkably high novelty, and they were predicted to infect ecologically important microbial clades, including Thaumarchaeota and Oleibacter. Significant inter-trench and intra-trench exchange of viral communities was proposed. Moreover, viral communities in different habitats (seawater/sediment and depth-stratified ocean zones) exhibited distinct niche-dependent distribution patterns and genomic properties. Notably, microbes and viruses in the hadopelagic seawater seemed to preferably adopt lysogenic lifestyles compared to those in the upper ocean. Furthermore, niche-specific auxiliary metabolic genes were identified in the hadal viral genomes, and a novel viral D-amino acid oxidase was functionally and phylogenetically characterized, suggesting the contribution of these genes in the utilization of refractory organic matter. Together, these findings highlight the genomic novelty, dynamic movement, and environment-driven diversification of viral communities in oceanic trenches, and suggest that viruses may influence the hadal ecosystem by reprogramming the metabolism of their hosts and modulating the community of keystone microbes.

Summary Shewanella strains are characterized by versatile metabolic capabilities, resulting in their wide distribution in the ocean at different depths. Considering that particle sedimentation is an important dynamic process in the ocean, we hypothesized that hadal Shewanella species evolved from the upper ocean. In this study, we isolated three novel Shewanella strains from deep‐sea sediments in the Southwest Indian Ocean. Genome sequencing indicated that strains YLB‐06 and YLB‐08 represent two novel species in the genus Shewanella. Through phylogenomic analysis, we showed that speciation and genomic changes in marine Shewanella strains are related to water depth. We further confirmed the aforementioned hypothesis and revealed a two‐stage process of the evolutionary transition of Shewanella from the upper ocean to the hadal zone by comparative genomics and gene gain/loss analysis. Finally, the transcriptomic analysis demonstrated that recently obtained genes are strictly repressed and may thus play a minor role in the response to environmental changes.

Phosphorothioate (PT) modification by the dnd gene cluster is the first identified DNA backbone modification and constitute an epigenetic system with multiple functions, including antioxidant ability, restriction modification, and virus resistance. Despite these advantages for hosting dnd systems, they are surprisingly distributed sporadically among contemporary prokaryotic genomes. To address this ecological paradox, we systematically investigate the occurrence and phylogeny of dnd systems, and they are suggested to have originated in ancient Cyanobacteria after the Great Oxygenation Event. Interestingly, the occurrence of dnd systems and prophages is significantly negatively correlated. Further, we experimentally confirm that PT modification activates the filamentous phage SW1 by altering the binding affinity of repressor and the transcription level of its encoding gene. Competition assays, concurrent epigenomic and transcriptomic sequencing subsequently show that PT modification affects the expression of a variety of metabolic genes, which reduces the competitive fitness of the marine bacterium Shewanella piezotolerans WP3. Our findings strongly suggest that a series of negative effects on microorganisms caused by dnd systems limit horizontal gene transfer, thus leading to their sporadic distribution. Overall, our study reveals putative evolutionary scenario of the dnd system and provides novel insights into the physiological and ecological influences of PT modification.

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Viruses, especially bacteriophages, are thought to have important functions in the deep-sea ecosystem, but little is known about the induction mechanism of benthic phages in response to environmental change. Our prior work characterized a cold-active filamentous phage SW1 that infects the deep-sea bacterium Shewanella piezotolerans WP3; however, the underlying mechanism of the putative thermo-regulated genetic switch of SW1 is still unclear. In this study, the DNA copy number and mRNA abundance of the deep-sea phage SW1 were quantified in the whole life cycle of its host S. piezotolerans WP3 at different temperatures. Our results demonstrated that the induction of SW1 is dependent on a threshold temperature (4°C), but this dependency is not proportional to temperature gradient. RNA-Seq analyses revealed two highly transcribed regions at 4°C and verified the presence of a long 3′ untranslated region (UTR) in the SW1 genome. Interestingly, recruitment analysis showed that SW1-like inoviruses prevail in deep sea (depth >1000 m) and photic epipelagic and mesopelagic zones (depth <1000 m), which suggested that the thermo-regulated genetic switch revealed in SW1 may be widely distributed in the ocean.