The deep-subseafloor biosphere harbours a major part of the total microbial biomass on Earth. However, how life and death in this environment are regulated is not yet understood. While organisms from higher trophic levels appear to be absent, viruses might be a factor for microbial mortality. In this study, we found an increasing ratio between viral and total cell counts with depth in deep-subseafloor sediments recovered during Leg 201 of the Ocean Drilling Program. A phylogenetically diverse culture collection from corresponding sediment layers was tested for the presence of inducible prophages. A treatment by mitomycin C as inducing agent indicated the presence of prophages in 46% of the bacterial isolates. Different morphotypes of myoviruses and siphoviruses were detected by transmission electron microscopy. Pulsed-field gel electrophoresis applied to viral DNA extracts showed their genetic diversity. Three host strains even harboured more than one prophage. Thus, our results prove the existence of functional viruses in the deep-subseafloor biosphere. Bacteriophages might take over the role of the main predators, as anoxia and oligotrophy favour the importance of viruses as mortality factors. Furthermore, the fact that the viral shunt recycles organic compounds might be of special relevance to this severely nutrient-depleted habitat.
Bacteriophages might be the main 'predators' in the marine deep subsurface and probably have a major impact on indigenous microbial communities. To identify their function within this habitat, we have determined their abundance and distribution along the sediment columns of two continental margin and two open ocean sites that were recovered during Leg 201 of the Ocean Drilling Program. For all investigated sites, viral abundance followed the total cell numbers with a virus-to-cell ratio between 1 and 10 in the upper 100 mbsf (meters below seafloor). An increasing ratio of about 20 in deeper layers indicated an ongoing viral production in up to 11 Ma old sediments. We have used Rhizobium radiobacter as the most frequently isolated organism from the deep subsurface with a high in situ abundance to identify the frequency of associated rhizobiophages. In this study, 16S rRNA gene copies of R. radiobacter accounted for up to 5.6% of total bacterial 16S rRNA genes (average: 0.75%) as detected by quantitative PCR. A distinctive distribution was identified for R. radiobacter as indicated by a site-specific arrangement of genetically similar populations. Whole genome information of rhizobiophage RR1-A was used to generate a primer system for quantitative PCR specifically targeting the prophage antirepressor gene, indicative for temperate phages. The quantification of this gene within various sediment horizons showed a contribution of temperate phages of up to 14.3% to the total viral abundance. Thus, the high amount of temperate phages within the sediments and among all investigated isolates indicates that lysogeny is the main viral proliferation mode in deep subsurface populations.
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