Flavobacteria blooms in four eutrophic lakes: linking population dynamics of freshwater bacterioplankton to resource availability

Abstract

Heterotrophic bacteria are major contributors to biogeochemical cycles and influence water quality. Still, the lack of representative isolates and the few quantitative surveys leave the ecological role and significance of single bacterial populations to be revealed. Here we analyzed the diversity and dynamics of freshwater Flavobacteria populations in four eutrophic temperate lakes. From each lake, clone libraries were constructed using primers specific for either the class Flavobacteria or Bacteria. Sequencing of 194 Flavobacteria clones from 8 libraries revealed a diverse freshwater Flavobacteria community and distinct differences among lakes. Abundance and seasonal dynamics of Flavobacteria were assessed by quantitative PCR with class-specific primers. In parallel, the dynamics of individual populations within the Flavobacteria community were assessed with terminal restriction fragment length polymorphism analysis using identical primers. The contribution of Flavobacteria to the total bacterioplankton community ranged from 0.4 to almost 100% (average, 24%). Blooms where Flavobacteria represented more than 30% of the bacterioplankton were observed at different times in the four lakes. In general, high proportions of Flavobacteria appeared during episodes of high bacterial production. Phylogenetic analyses combined with Flavobacteria community fingerprints suggested dominance of two Flavobacteria lineages. Both drastic alterations in total Flavobacteria and in community composition of this class significantly correlated with bacterial production, emphasizing that resource availability is an important driver of heterotrophic bacterial succession in eutrophic lakes.

FIG. 1.

Flavobacterial 16S rRNA genes as a percentage of total bacterial 16S rRNA genes (% Flavobacteria; bars), changes in bacterial production (filled circles), and chlorophyll a (open squares) in four lakes. All values are averages from triplicate analyses, and error bars indicate standard deviations.

FIG. 2.

Rarefaction analyses of the eight clone libraries based on high-resolution terminal restriction fragment length polymorphism screening. Two clone libraries using either universal primers (27f and 1492r) or flavobacterium-specific primers (27f and 588r) are plotted in each graph.

FIG. 3.

Temporal dynamics of dominant operationally defined Flavobacteria populations (terminal restriction fragments B86, B88, B90, and B99) and sum of all other peaks (remaining) from T-RFLP profiles of HhaI-digested PCR-amplified DNA from four lakes. y axis represents relative peak intensity multiplied by relative contribution of Flavobacteria to the total bacterial community. Phylogeny of each terminal restriction fragment is shown in Fig. S1 in the supplemental material.

FIG. 4.

Cluster analysis of flavobacterial communities. Unweighted pair-grouped tree diagram of 24 samples that were analyzed by T-RFLP fingerprinting and subsequent statistical analyses as described elsewhere (8).