Mixing alters the lytic activity of viruses in the dark ocean.

Christian Winter,Thomas Reinthaler,Nicole Köstner,Gerhard J Herndl,Damaris Urban,Carl-Philip Kruspe,Simone Muck

doi:10.1002/ecy.2135

Abstract

In aquatic habitats, viral lysis of prokaryotic cells lowers the overall efficiency of the microbial loop, by which dissolved organic carbon is transfered to higher trophic levels. Mixing of water masses in the dark ocean occurs on a global scale and may have far reaching consequences for the different prokaryotic and virus communities found in these waters by altering the environmental conditions these communities experience. We hypothesize that mixing of deep ocean water masses enhances the lytic activity of viruses infecting prokaryotes. To address this hypothesis, major deep‐sea water masses of the Atlantic Ocean such as North Atlantic Deep Water, Mediterranean Sea Overflow Water, Antarctic Intermediate Water, and Antarctic Bottom Water were sampled at five locations. Prokaryotic cells from these samples were collected by filtration and subsequently incubated in virus‐reduced water from either the same (control) or a different water mass (transplantation treatment). Additionally, mixtures of prokaryotes obtained from two different water masses were incubated in a mixture of virus‐reduced water from the same water masses (control) or in virus‐reduced water from the source water masses separately (mixing treatments). Pronounced differences in productivity‐related parameters (prokaryotic leucine incorporation, prokaryotic and viral abundance) between water masses caused strong changes in viral lysis of prokaryotes. Often, mixing of water masses increased viral lysis of prokaryotes, indicating that lysogenic viruses were induced into the lytic cycle. Mixing‐induced changes in viral lysis had a strong effect on the community composition of prokaryotes and viruses. Our data show that mixing of deep‐sea water masses alters levels of viral lysis of prokaryotes and in many cases weakens the efficiency of the microbial loop by enhancing the recycling of organic carbon in the deep ocean.

Highlights

The composition of prokaryotic and virus communities changes throughout the oceanic water column (Galand et al 2010, Agogue et al 2011, Winter et al 2013, Hurwitz et al 2014) because the ocean is vertically structured
In most cases mixing increased Frequency of infected cells (FIC) and viral production (VP) there was no evidence that differences in prokaryotic growth rates caused these changes
Changes in FIC and VP were largely independent of the identity of the source water masses and, of the composition of prokaryotic and viral communities

Summary

Introduction

The composition of prokaryotic (members of the domains Bacteria and Archaea, no phylogenetic relationship is implied) and virus communities changes throughout the oceanic water column (Galand et al 2010, Agogue et al 2011, Winter et al 2013, Hurwitz et al 2014) because the ocean is vertically structured. The sunlit surface layer is separated by a thermocline from the deep ocean (>200 m depth). Given that temperature and the concentration of dissolved salts (salinity) determine the density of water, the sunlit water above the thermocline is warmer and, lighter compared to the water below it. The deep ocean is separated from the atmosphere by a thin layer of lighter and warmer surface water and is considered to be a stable ecosystem, where changes are presumed to occur on the scale of years to decades (e.g., Bethoux et al 1990) rather than weeks to months. The deep ocean itself is vertically-structured due to fine-grained differences in temperature and salinity resulting in subtle density differences that give rise to defined water masses (Emery 2001) and harbor distinct prokaryotic and Manuscript received 5 July 2017; revised October 2017; accepted December 2017.

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Discussion

Conclusion