Abstract

The current consensus concerning the viral regulation of prokaryotic carbon metabolism is less well-studied, compared to substrate availability. We explored the seasonal and vertical distribution of viruses and its relative influence on prokaryotic carbon metabolism in a hypereutrophic reservoir, Lake Villerest (France). Flow cytometry and transmission electron microscopy (TEM) analyses to determine viral abundance (VA; range = 6.1–63.5 × 107 ml-1) and viral infection rates of prokaryotes (range = 5.3–32%) respectively suggested that both the parameters varied more significantly with depths than with seasons. Prokaryotic growth efficiency (PGE, considered as a proxy of prokaryotic carbon metabolism) calculated from prokaryotic production and respiration measurements (PGE = prokaryotic production/[prokaryotic production + prokaryotic respiration] × 100) varied from 14 to 80% across seasons and depths. Viruses through selective lyses had antagonistic impacts on PGE by regulating key prokaryotic metabolic processes (i.e., production and respiration). Higher viral lysis accompanied by higher respiration rates and lower PGE in the summer (mean = 22.9 ± 10.3%) than other seasons (mean = 59.1 ± 18.6%), led to significant loss of carbon through bacterial-viral loop and shifted the reservoir system to net heterotrophy. Our data therefore suggests that the putative adverse impact of viruses on the growth efficiency of the prokaryotic community can have strong implications on nutrient flux patterns and on the overall ecosystem metabolism in anthropogenic dominated aquatic systems such as Lake Villerest.

Highlights

  • Heterotrophic prokaryotes are a prime biological component of the biosphere and account for a significant fraction of plankton biomass in aquatic systems

  • Water temperature in the epilimnion (0.5 m depth) showed seasonal changes (p < 0.001); the values increased from 11.8◦C (April) to 25.2◦C (July) and gradually decreased to 11.8◦C toward end of study period in November (Figure 1A)

  • The present investigation is one of the few that reveals some notable features regarding the potential links between viral infection and prokaryotic community metabolism in addition to environmental factors affecting the seasonal standing stocks of viruses and lytic phage infection in the water column of hyper eutrophic Villerest reservoir

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Summary

Introduction

Heterotrophic prokaryotes are a prime biological component of the biosphere and account for a significant fraction of plankton biomass in aquatic systems Factors that control their abundance and activity are crucial to understand their role in the biogeochemical cycles, the fate of organic carbon and nutrients, and the flow of energy to higher trophic levels (Azam and Malfatti, 2007). Prokaryotic growth efficiency was largely thought to be controlled by bottom–up factors (substrate supply), but with the recognition of viruses as dynamic components of planktonic communities in a wide variety of aquatic systems our conceptual understanding of the structural and functional organization of aquatic microbial food webs has changed (Suttle, 2007; Breitbart, 2012; Sime-Ngando, 2014). Few quantitative data have been published on the above issue and many questions remain unanswered

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