High virus-to-cell ratios indicate ongoing production of viruses in deep subsurface sediments

Abstract

Marine sediments cover two-thirds of our planet and harbor huge numbers of living prokaryotes. Long-term survival of indigenous microorganisms within the deep subsurface is still enigmatic, as sources of organic carbon are vanishingly small. To better understand controlling factors of microbial life, we have analyzed viral abundance within a comprehensive set of globally distributed subsurface sediments. Phages were detected by electron microscopy in deep (320 m below seafloor), ancient (B14 Ma old) and the most oligotrophic subsurface sediments of the world's oceans (South Pacific Gyre (SPG)). The numbers of viruses (10 4 -10 9 cm À 3 , counted by epifluorescence microscopy) generally decreased with sediment depth, but always exceeded the total cell counts. The enormous numbers of viruses indicate their impact as a controlling factor for prokaryotic mortality in the marine deep biosphere. The virus-to-cell ratios increased in deeper and more oligotrophic layers, exhibiting values of up to 225 in the deep subsurface of the SPG. High numbers of phages might be due to absorption onto the sediment matrix and a diminished degradation by exoenzymes. However, even in the oldest sediments, microbial communities are capable of maintaining viral populations, indicating an ongoing viral production and thus, viruses provide an independent indicator for microbial life in the marine deep biosphere.

Microbial community assembly in marine sediments

“…In theory, the rates of diversification could be amplified by different factors, such as the propensity for microorganisms to acquire genes from other organisms through HGT (Wiedenbeck & Cohan 2011). Since viruses appear to be highly abundant in subsurface sediments, they could act to accelerate rates of HGT (Engelhardt et al 2014(Engelhardt et al , 2015. However, due to the apparent lack of longdistance dispersal in the subsurface, HGT would be more likely to act within localized populations and would not contribute significantly to the broad patterns of vertical distribution that we see (Fig.…”

“…Functional differences among taxa may also represent selection pressures other than, or in addition to, energy limitation. The most notable of these is viral-induced cell death, which has been suggested to be a significant contributor to cellular mortality in the deep subsurface (Danovaro et al 2008, Engelhardt et al 2014, 2015, Jørgensen & Marshall 2016. Resistance to viral lysis could mediate the selective survival of key taxa in the sediment column while also playing an important role in altering the subsurface environment.…”

Marine Viruses: the Beneficial Side of a Threat

“…Marine viruses comprise approximately 94 % of the nucleic acid-containing particles in the oceans, while prokaryotes and protists represent only a 5 and 1 %, respectively. Similarly, the number of viruses in marine sediments always exceeds the total cell counts [63]. The extensive number of viruses in marine sediments highlights their impact as a controlling factor for prokaryotic mortality.…”

Spatial and temporal dynamics of virioplankton in a high mountain tropical reservoir, El Neusa (Cundinamarca, Colombia)

“…So far, it is known that viruses are the most abundant biological entities in the water column and sediment, both in freshwater and marine systems (Fuhrman, 1999;Bettarel et al, 2003;Engelhardt et al, 2014). They infect a wide spectrum of hosts ranging from prokaryotes (e.g., bacteria and archaea) to unicellular and multicellular eukaryotes, and therefore are considered as a controlling factor of both the abundance and the genetic diversity of populations (Brussaard, 2004;Suttle, 2007;Fischer et at., 2010).…”