Viral Regulation of Prokaryotic Carbon Metabolism in a Hypereutrophic Freshwater Reservoir Ecosystem (Villerest, France)

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 × 10(7) 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.

Keywords: Villerest reservoir; lytic infection; prokaryotes; prokaryotic growth efficiency; seasonal dynamics; viruses.

FIGURE 1

Spatio-temporal variation of (A) water temperature and (B) dissolved oxygen concentration in the water column of Villerest reservoir from April to November 2012.

FIGURE 2

Spatio-temporal variability in (A) viral abundance, (B) prokaryote abundance, and (C) virus to prokaryote ratio in the water column of Villerest reservoir, April–November 2012. Error bars are SE.

FIGURE 3

Estimates of (A) prokaryotic growth efficiency, (B) the relation between prokaryotic production and respiration (PR = -0.03PP² + 0.18PP + 10.67, r = -0.51, p < 0.01), and (C) prokaryotic growth efficiency and production (PGE = 11.63 × 0.64, r = 0.83, p < 0.001) in Villerest reservoir. For seasonal variability and scatter plot diagram, data on PR and production (used to calculate prokaryotic growth efficiency) was not included during the period of anoxia that was observed in certain months at metalimnion and hypolimnion. Error bars are SE.

FIGURE 4

Spatio-temporal variability in the (A) frequency of infected cells (FICs), (B) FICs (percentage of total infected cells), and (C) maximum burst size estimates (viruses per prokaryote) for different prokaryote morphotypes. Error bars are SE.

FIGURE 5

Relationship between viral infected prokaryotic cells and prokaryotic growth efficiency (log PGE = -1.94 × log(FIC)² + 3.77 × log(FIC) + 0.09, r = -0.69, p < 0.001) in Villerest reservoir.