Extracellular DNA can preserve the genetic signatures of present and past viral infection events in deep hypersaline anoxic basins

Abstract

Deep hypersaline anoxic basins (DHABs) of the Mediterranean Sea are among the most extreme ecosystems on Earth and host abundant, active and diversified prokaryotic assemblages. However, factors influencing biodiversity and ecosystem functioning are still largely unknown. We investigated, for the first time, the impact of viruses on the prokaryotic assemblages and dynamics of extracellular DNA pool in the sediments of La Medee, the largest DHAB found on Earth. We also compared, in La Medee and L'Atalante sediments, the diversity of prokaryotic 16S rDNA sequences contained in the extracellular DNA released by virus-induced prokaryotic mortality. We found that DHAB sediments are hot-spots of viral infections, which largely contribute to the release of high amounts of extracellular DNA. DNase activities in DHAB sediments were much higher than other extracellular enzymatic activities, suggesting that extracellular DNA released from killed prokaryotes can be the most suitable trophic resource for benthic prokaryotes. Preserved extracellular DNA pools, which contained novel and diversified gene sequences, were very similar between the DHABs but dissimilar from the respective microbial DNA pools. We conclude that the strong viral impact in DHAB sediments influences the genetic composition of extracellular DNA, which can preserve the signatures of present and past infections.

Keywords: deep hypersaline anoxic basins; extracellular DNA; prokaryotes; viruses.

Figure 1.

Viral abundance in (a) surface (0–1 cm) and (b) subsurface (down to 10–15 cm) sediments of La Medee basin and oxic station. Prokaryotic abundance in (c) surface (0–1 cm) and (d) subsurface (down to 10–15 cm) sediments of La Medee basin and oxic station. Standard deviations (n = 3) are reported.

Figure 2.

Viral production and decay in surface sediments (0–1 cm) of La Medee and oxic station. Standard deviations (n = 3) are reported.

Figure 3.

Simplified scheme showing the impact of the viral lysis on prokaryotic dynamics in DHAB sediments. The values of prokaryotes produced per gram of sediment and per hour are based on the determination of prokaryotic heterotrophic C production.

Figure 4.

Total extracellular DNA concentrations in (a) surface (0–1 cm) and (b) subsurface (down to 10–15 cm) sediments of La Medee and oxic station. Standard deviations (n = 3) are reported.

Figure 5.

DNase activity in (a) surface (0–1 cm) and (b) subsurface (down to 10–15 cm) sediments of La Medee and oxic station. Standard deviations (n = 3) are reported.

Figure 6.

Contribution of different bacterial classes to the total bacterial assemblages associated with extracellular DNA and microbial DNA in La Medee, L'Atalante and oxic sediments.