Bloom of filamentous bacteria in a mesotrophic lake: identity and potential controlling mechanism

Abstract

Ephemeral blooms of filamentous bacteria are a common phenomenon in the water column of oligo- to mesotrophic lakes. It is assumed that the appearance of such morphotypes is favored by selective predation of bacterivorous protists and that filter-feeding zooplankton plays a major role in suppressing these bacteria. The phylogenetic affiliation of the important bloom-forming filamentous bacteria in freshwaters is presently unknown. Here we report the identification of dominant members of a filamentous bacterial assemblage during a bloom of such morphotypes in a mesotrophic lake. By molecular cloning and fluorescence in situ hybridization with specific oligonucleotide probes, up to 98% of filamentous cells in lake water could be assigned to a clade of almost identical (99% similarity) 16S rRNA gene sequence types, the cosmopolitan freshwater LD2 cluster. For a period of less than 1 week, members of the LD2 clade constituted >40% of the total bacterial biomass, potentially favored by high grazing of planktivorous protists. This is probably the most pronounced case of dominance by a single bacterioplankton species ever observed in natural freshwaters. In enclosures artificially stocked with the metazoan filter feeder Daphnia, bacteria related to the LD2 clade formed a significantly larger fraction of filaments than in enclosures where Daphnia had been removed. However, in the presence of higher numbers of Daphnia individuals, the LD2 bacteria, like other filaments, were eventually eliminated both in enclosures and in the lake. This points at the potential importance of filter-feeding zooplankton in controlling the occurrence and species composition of filamentous bacterial morphotypes in freshwater plankton.

FIG. 1.

Development of the microbial assemblages in Schöhsee during the study period. Panels: a, abundances of heterotrophic nanoflagellates (HNF) and ciliates; b, total bacterial numbers and [³H]thymidine uptake rate; c, abundances and biovolume of filamentous bacterial morphotypes; d, relative contributions of three size fractions to the biovolume of filamentous bacteria.

FIG. 2.

Biovolumes of filamentous bacteria that developed in replicate lake water mesocosms that had been stocked with different Daphnia densities 2 weeks earlier. Ind. L⁻¹, individuals per liter.

FIG. 3.

(Upper panels) Dynamics of heterotrophic nanoflagellates (HNF) and ciliates in experimental mesocosms either seeded with 5 Daphnia individuals liter⁻¹ (+Daphnia) or without zooplankton (control). (Lower panels) Abundances and biovolumes of filamentous bacterial morphotypes.

FIG. 4.

Phylogenetic positions of 16S rDNA sequences from Schöhsee affiliated with the Cytophaga-Flavobacterium lineage of the phylum Bacteroidetes. Only some of the nearly identical clones are depicted. The brackets indicate sequences targeted by newly designed specific FISH probes LD2-739 and CL500-653. Bar, 10% estimated sequence divergence.

FIG. 5.

Photomicrographs of common and rare filamentous bacteria hybridized with probes for different lineages of the Cytophaga-Flavobacteria cluster. Left panels, hybridized cells (arrows); right panels, same microscopic field, all cells (DAPI staining). Panels: a and b, probe LD2-739; c and d, probe CL500-653; e and f, probe R-FL615. Bar, 10 μm. Other orange fluorescent objects visible in the panels are cyanobacteria and algal plastids.

FIG. 6.

(a) Cell numbers of filaments hybridized with probe LD2-739 in Schöhsee and their mean fraction of the total bacterial biovolume (+1 standard deviation). (b) Cell length distributions of filaments related to the LD2 clade at different sampling dates. Box plots depict medians and 50th, 75th, and 90th percentiles. Asterisks indicate dates with significant differences from the first sampling date.

FIG. 7.

Development of relative (a) and absolute (b) abundances of filaments related to the LD2 clade in mesocosms with and without Daphnia. The treatment definitions are given in the legend to Fig. 3.