Active and diverse viruses persist in the deep sub-seafloor sediments over thousands of years

Abstract

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.

Fig. 1

Depth profiles of viral abundance, prokaryotic abundance, virus-to-prokaryote ratio (VPR) and total organic carbon (TOC) in sediment cores from four Baltic Sea holes. The data for TOC is from ref. . Note different scales

Fig. 2

Apparent production of viruses in the sediments. (a), Depth profiles of apparent lytic (red circles) and inducible lysogenic (blue circles) viral production in the sediments at Hole M59C. (b), Relationships between lytic and lysogenic viral production and prokaryotic abundance. The red line represents the linear regression between lytic viral production and prokaryotic abundance

Fig. 3

Transmission electron micrographs showing the morphologies of virus-like particles and infected cells in the deep sediments of the Baltic Sea. (a), Examples of virus-like particles observed. Scale bars: 100 nm. (b), Infective viruses (arrows) in the visibly infected cells. Samples were recovered from deep sediments down to 70 mbsf in Hole M59C

Fig. 4

Maximum-likelihood phylogenetic analysis based on major g23 OTUs of amino acid sequences. OTUs with relative abundances >1% in each sample (a total of 84 OTUs) from Holes M59C and M63E of the Baltic Sea sediment were selected. Different colored ranges indicate g23 sequences from different groups or origins. Reference sequences are in bold text. Black and red dots show internal nodes with a >50% and >80% bootstrap (1000-fold replicated) support, respectively. The outer colored rings indicate the relative abundance of sequences of each OTU in each sample. Light gray indicates sequences undetected in the samples (relative abundance of 0%)

Fig. 5

Relationships between (a) viral abundance and prokaryotic abundance, (b) virus to prokaryote ratio (VPR) and total organic carbon (TOC), and (c) viral abundance and potential lytic or inducible lysogenic viral production