Viruses are ubiquitous and cause significant mortality in marine bacterial and archaeal communities. Little is known about the role of viruses in the sub-seafloor biosphere, which hosts a large fraction of all microbes on Earth. We quantified and characterized viruses in sediments from the Baltic Sea. The results show that the Baltic Sea sub-seafloor biosphere harbors highly abundant viruses with densities up to 1.8 × 1010 viruses cm−3. High potential viral production down to 37 meters below seafloor in ca. 6000-years-old sediments and infected prokaryotic cells visible by transmission electron microscopy demonstrate active viral infection. Morphological and molecular data indicate that the highly diverse community of viruses includes both allochthonous input from the overlying seawater and autochthonous production. The detection of cyanophage-like sequences showed that viruses of phototrophic hosts may persist in marine sediments for thousands of years. Our results imply that viruses influence sub-seafloor microbial community dynamics and thereby affect biogeochemical processes in the sub-seafloor biosphere.

Summary As the most abundant and genetically diverse biological entities, viruses significantly influence ecological, biogeographical and evolutionary processes in the ocean. However, the biogeography of marine viruses and the drivers shaping viral community are unclear. Here, the biogeographic patterns of T4‐like viruses and the relative impacts of deterministic (environmental selection) and dispersal (spatial distance) processes were investigated in the northern South China Sea. The dominant viral operational taxonomic units were affiliated with previously defined Marine, Estuary, Lake and Paddy Groups. A clear viral biogeographic pattern was observed along the environmental gradient from the estuary to open sea. Marine Groups I and IV had a wide geographical distribution, whereas Marine Groups II, III and V were abundant in lower‐salinity continental or eutrophic environments. A significant distance‐decay pattern was noted for the T4‐like viral community, especially for those infecting cyanobacteria. Both deterministic and dispersal processes influenced viral community assembly, although environmental selection (e.g. temperature, salinity, bacterial abundance and community, etc.) had a greater impact than spatial distance. Network analysis confirmed the strong association between viral and bacterial community composition, and suggested a diverse ecological relationship (e.g. lysis, co‐infection or mutualistic) between and within viruses and their potential bacterial hosts.

Cyanopodoviruses affect the mortality and population dynamics of the unicellular picocyanobacteria Prochlorococcus and Synechococcus, the dominant primary producers in the oceans. Known cyanopodoviruses all contain the DNA polymerase gene (DNA pol) that is important for phage DNA replication and widely used in field quantification and diversity studies. However, we isolated 18 cyanopodoviruses without identifiable DNA pol. They form a new MPP-C clade that was separated from the existing MPP-A, MPP-B, and P-RSP2 clades. The MPP-C phages have the smallest genomes (37.3–37.9 kb) among sequenced cyanophages, and show longer latent periods than the MPP-B phages. Metagenomic reads of both clades are highly abundant in surface waters, but the MPP-C phages show higher relative abundance in surface waters than in deeper waters, while MPP-B phages have higher relative abundance in deeper waters. Our study reveals that cyanophages with distinct genomic contents and infection kinetics can exhibit different depth profiles in the oceans.