Bottom-up versus top-down control of hypo- and epilimnion free-living bacterial community structures in two neighboring freshwater lakes

Abstract

Bacterioplankton plays a central role in the microbial functioning of lacustrine ecosystems; however, factors that constrain its structural variation are still poorly understood. Here we evaluated the driving forces exerted by a large set of environmental and biological parameters on the temporal and spatial dynamics of free-living bacterial community structures (BCS) in two neighboring perialpine lakes, Lake Bourget and Lake Annecy, which differ in trophic status. We analyzed monthly data from a 1-year sampling period at two depths situated in the epi- and hypolimnia for each lake. Overall, denaturing gradient gel electrophoresis (DGGE) revealed significant differences in the BCS in the two lakes, characterized by a higher number of bands in the oligotrophic ecosystem (i.e., Lake Annecy). The temporal dynamics of BCS differed greatly between depths and lakes, with temporal scale patterns being much longer in the mesotrophic Lake Bourget. Direct-gradient multivariate ordination analyses showed that a complex array of biogeochemical parameters was the driving force behind BCS shifts in both lakes. Our results indicated that 60 to 80% of the variance was explained only by the bottom-up factors in both lakes, indicating the importance of nutrients and organic matter from autotrophic origin in controlling the BCS. Top-down regulation by flagellates together with ciliates or viruses was found only in the hypolimnion and not in the epilimnion for both lakes and explained less than 18% of the bacterial community changes during the year. Our study suggests that the temporal dynamics of the free-living bacterial community structure in deep perialpine lakes are dependent mainly on bottom-up factors and to a lesser extent on top-down factors, whatever the specific environmental conditions of these lakes.

Fig. 1.

Temporal evolution of temperatures in Lakes Bourget (2 m versus 50 m) and Annecy (3 m versus 45 m) in 2007.

Fig. 2.

Dendrogram obtained by UPGMA clustering of DGGE banding patterns from Lakes Bourget (A) and Annecy (B). Similarity is expressed as a percentage of the Bray-Curtis index.

Fig. 3.

Canonical correspondence analysis of the bacterioplankton community structure from samples in Lake Bourget (A and B) and Lake Annecy (C and D) at 2 m (A) versus 50 m (B) and at 3 m (C) versus 45 m (D), respectively, using physicochemical and biological parameters. Arrows point in the direction of increasing values of each variable. The length of the arrow indicates the degree of correlation with the represented axes. The position of samples relative to arrows is interpreted by projecting the points on the arrow and indicates the extent to which a sample bacterial community structure is influenced by the environmental parameter represented by that arrow. Chl a, chlorophyll a; Temp, Temperature; O₂, dissolved oxygen; NH₄, ammonium; NO₃, nitrates; Pt, total phosphorus; SiO₂, silicates; PNF, pigmented nanoflagellates; HNF, heterotrophic nanoflagellates.

Fig. 4.

Variation partitioning analysis of 16S rRNA gene data sets from Lake Bourget (A and B) and Lake Annecy (C and D) at 2 m (A) versus 50 m (B) and at 3 m (C) versus 45 m (D), respectively. Pure bottom-up variables were nitrate, ammonium, total phosphorus, and silicates. In Lake Bourget, physicochemical parameters were temperature, nitrate, ammonium, and total phosphorus for 2-m samples and nitrate, ammonium, total phosphorus, silicate, dissolved oxygen, and chlorophyll a for 50-m samples. Apparent top-down variables were ciliate and HNF abundances at 50 m. In Lake Annecy, physicochemical factors were nitrate, total phosphorus, silicates, dissolved oxygen, and chlorophyll a for 3-m samples and temperature, silicate, nitrate, ammonium, total phosphorus, dissolved oxygen, and chlorophyll a for 45-m samples. Pure bottom-up factors were PNF and viruses at 3 m and HNF and viruses at 45 m. For each data set, P < 0.01.