Diversity and distribution of viruses inhabiting the deepest ocean on Earth

Abstract

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.

Isolation and characterization of a novel linear-plasmid phage from the sediment of the Mariana Trench

“…With a water depth >6000 ​m, the hadal zone represents one of the least-studied environments on the planet, and it is an indispensable part of the ocean ( Jamieson et al., 2010 ). A recent study has shown that hadal viruses (mainly bacteriophages) harbor unprecedented genomic novelty and are ecologically important ( Jian et al., 2021 ). Nevertheless, only a single phage, PstS-1, was previously isolated from the abyssal environment (the seawater of the Japan Trench at a depth of 7000 m) ( Yoshida et al., 2015 ).…”

Novel Viral Communities Potentially Assisting in Carbon, Nitrogen, and Sulfur Metabolism in the Upper Slope Sediments of Mariana Trench

“…In fact, the discovery of Phycodnaviridae viruses in the sediments of the Mariana Trench is not unusual. The sequences of eukaryotic algal viruses have also been detected in the Baltic Sea subseafloor sediments ( 47 ), the sediments of Loki’s Castle hydrothermal vent (∼3,200 m below sea level) in the mid-Atlantic Ocean ( 29 ), and the abyssopelagic Yap Trench sediments ( 48 ). The presence of phytoplankton viruses might be explained if viruses cosink with eukaryotic phytoplankton from the upper water column via the sinking mechanism of the biological pump ( 47 , 49 ).…”

“…Besides, BLAST analysis of viral scaffolds was also performed against the Integrated Microbial Genome/Virus (IMG/VR) system v.3.0 database ( 88 ) (BLASTn E value of ≤10 −5 , similarity of ≥90%, and covered length of ≥75%) to assign the taxonomies for viral scaffolds based on sequence similarity ( 49 , 83 ). Additionally, a majority-rules approach was performed for the taxonomic assignments as previously described ( 48 , 88 ). Briefly, predicted proteins from viral scaffolds were compared to NCBI viral RefSeq proteins (release 203) using DIAMOND v2.0.4 ( 89 ) (BLASTp; -subject-cover 50; –more-sensitive; -query-cover 50; -evalue 1e-5), and a viral scaffold was assigned to a taxonomy if ≥50% of the proteins were assigned to that taxonomy.…”

“…Provirus-like viral scaffolds were predicted by BLAST analysis against the microbial bins (BLASTn E value of 10 −3 , 70% similarity, and 75% of the viral scaffold length) ( 98 ) and using PHISDector ( 96 ), CheckV v0.7.0 ( 87 ), and VIBRANT v1.2.1 ( 99 ). In addition, viral scaffolds harboring lysogenic marker proteins, such as integrase, excisionase, invertase, serine recombinase, and CI/Cro repressor ( 48 , 100 , 101 ), are considered potential proviruses.…”

Diversity of Giant Viruses Infecting Vermamoeba vermiformis

“…This has broadened our understanding of the viral world, especially of viruses that infect microbes. It is now universally recognized that viruses are the most abundant biological entities on the Earth ( Jian et al, 2021 ) and have contributed substantially to the evolution of life. In this general context, the scientific community began to take an interest in amoeba viruses in the early 2000s.…”