Members of a readily enriched beta-proteobacterial clade are common in surface waters of a humic lake

Abstract

Humic lakes are systems often characterized by irregular high input of dissolved organic carbon (DOC) from the catchment. We hypothesized that specific bacterial groups which rapidly respond to changes in DOC availability might form large populations in such habitats. Seasonal changes of microbial community composition were studied in two compartments of an artificially divided bog lake with contrasting DOC inputs. These changes were compared to community shifts induced during short-term enrichment experiments. Inocula from the two compartments were diluted 1:10 into water from the more DOC-rich compartment, and inorganic nutrients were added to avoid microbial N and P limitation. The dilutions were incubated for a period of 2 weeks. The microbial assemblages were analyzed by cloning and sequencing of 16S rRNA genes and by fluorescence in situ hybridization with specific oligonucleotide probes. beta-Proteobacteria from a cosmopolitan freshwater lineage related to Polynucleobacter necessarius (beta II) were rapidly enriched in all treatments. In contrast, members of the class Actinobacteria did not respond to the enhanced availability of DOC by an immediate increase in growth rate, and their relative abundances declined during the incubations. In lake water members of the beta II clade seasonally constituted up to 50% of all microbes in the water column. Bacteria from this lineage annually formed a significantly higher fraction of the microbial community in the lake compartment with a higher allochthonous influx than in the other compartment. Actinobacteria represented a second numerically important bacterioplankton group, but without clear differences between the compartments. We suggest that the pelagic microbial community of the studied system harbors two major components with fundamentally different growth strategies.

FIG. 1.

Schematic depiction of the compartments of Lake Groβe Fuchskuhle in relationship to the area of water in- and outflow of the catchment. The inflow area is largely formed by a Sphagnum bog. Contour lines indicate a 0.1-m change in altitude.

FIG. 2.

Phylogenetic relationship of β-proteobacterial 16S rRNA gene sequences from the study system and from enrichments of prefiltered (pore size, 0.1 μm) water from the SW compartment (1:10 dilutions). Sequences originating from Lake Groβe Fuchskuhle are depicted in boldface type, and sequences produced during this study are underlined. The scale bar indicates 10% estimated sequence divergence.

FIG. 3.

Development of total bacterial abundances (a) and bacterial [³H]leucine incorporation (b) during the enrichment experiments. For the SW and NE treatments, inocula from the SW and NE compartments, respectively, were diluted 1:10 into prefiltered (pore size, 0.1 μm) water from the SW compartment.

FIG. 4.

Relative abundances of members of the class Actinobacteria and of the beta II clade (bacteria related to P. necessarius) during the enrichment on prefiltered (pore size, 0.1 μm) water from the SW compartment. (a and b) Inocula from the SW (a) and NE (b) compartments.

FIG. 5.

Relative abundances of β-proteobacteria and of members of the beta II clade in surface waters of the SW and NE compartments of Lake Groβe Fuchskuhle between September 2000 and September 2001.

FIG. 6.

Relative abundances of Actinobacteria in surface waters of the SW and NE compartments of Lake Groβe Fuchskuhle between September 2000 and September 2001.

FIG. 7.

Ratios of members of the beta II clade to Actinobacteria in surface waters of the SW and NE compartments of Lake Groβe Fuchskuhle between September 2000 and September 2001.