Quantitative dominance of seasonally persistent filamentous cyanobacteria (Planktothrix rubescens) in the microbial assemblages of a temperate lake

The spatiotemporal changes in abundance and biomass of heterotrophic bacteria, of three major bacterial phylogenetic groups, and of picocyanobacteria in the upper 20 m of a deep prealpine lake (Lake Zurich, Switzerland) were monitored during a seasonally persistent bloom of the toxigenic filamentous cyanobacterium Planktothrix rubescens. In addition, bacterial 16S ribosomal deoxyribonucleic acid (rDNA) sequences were collected at one instance from the bloom layer and from waters above and below this zone. P. rubescens comprised up to 70% of particulate organic carbon during summer stratification and autumnal mixis and thus by far exceeded the total biomass both of other phytoplankton and of prokaryotes. A strong negative correlation was found between the estimated basin-wide biomass of P. rubescens and of heterotrophic bacteria, and there was different spatial niche preference of filamentous vs. picocyanobacteria. Only members of the Cytophaga– Flavobacterium lineage of Bacteroidetes showed an increasing tendency of association with the P. rubescens population, in particular at the onset of autumnal mixing. Although the filamentous cyanobacterium was the dominant primary producer throughout the year, it did not seem to be a carbon source for heterotrophic bacteria at all. We conclude that P. rubescens represents a powerful competitor of autotrophic and heterotrophic prokaryotes, likely due to both its specific physiological (photoheterotrophic) properties and its protection against zooplankton grazing. This competitiveness might be regarded as another reason for its mass occurrence in numerous lakes of the Northern hemisphere. Autotrophic and heterotrophic microorganisms in the plankton of lakes and oceans are connected by multifarious relationships. Heterotrophic bacteria profit from organic substrates fixed by the phytoplankton and released during nutrient limited growth (Børsheim et al. 2005) or upon disintegration of algal cells. At the same time, the two groups compete for growth-limiting nutrients, e.g., for phosphorus in freshwater systems (Løvdal et al. 2007), with heterotrophic bacteria being more effective than algae at low nutrient concentrations (Mindl et al. 2005). The interactions between heterotrophic bacteria and primary producers in freshwaters have mainly been investigated in the context of artificially induced (Riemann and Søndergaard 1986) or natural (Zeder et al. 2009) shortlived blooms of prokaryotic and eukaryotic phytoplankton species. The typically observed patterns, e.g., during phytoplankton spring blooms, are an increase of dissolved organic carbon and of bacterial cell numbers and activity (Simon et al. 1998) during or after the maximum concentrations of chlorophyll a (Chl a) and a subsequent formation of macroscopic organic aggregates (due to the agglutination of senescent algae) colonized by bacteria that differ from single-celled planktonic taxa (Grossart et al. 1997; Schweitzer et al. 2001). Such transient phytoplankton blooms are often accompanied by pronounced changes in microbial community composition, e.g., a disproportionate rise of bacteria affiliated with Flavobacteria (Zeder et al. 2009), Betaproteobacteria (Salcher et al. 2008), or Actinobacteria (Salcher et al. 2010). By contrast, considerably less is known about the coexistence of bacteria with phytoplankton groups that are seasonally more persistent (Šimek et al. 2008). The filamentous cyanobacterium Planktothrix rubescens is the dominant primary producer in the mesotrophic, prealpine Lake Zurich, Switzerland (Micheletti et al. 1998). A mass occurrence of this species has also been observed in numerous other lakes of the Northern Hemisphere (Ernst et al. 2009). Typically, the population is established in the metalimnion during early summer, where it forms an increasingly concentrated layer. Upon the onset of autumnal mixing it is dispersed throughout the epilimnetic water body and subsequently transported through the deepening mixed zone (Micheletti et al. 1998). P. rubescens can account for half of the total phytoplankton biomass in Lake Zurich in summer and for even more during the autumn and winter months. Several ecophysiological traits enhance the competitive abilities of this cyanobacterium in stratified lakes compared with other prokaryotic and eukaryotic phytoplankton species, such as adaptation to low irradiance and temperatures (Walsby and Schanz 2002), harmful secondary metabolites (Blom et al. 2006), or gas vesicles that allow filaments to regulate their vertical position within the stratified water column (Walsby et al. 1998). Planktothrix spp. are among the most important producers of hepatotoxic microcystins in freshwaters (Kurmayer and Gumpenberger 2006), which effectively provides a population-level protection against zooplankton grazing (Kurmayer and Jüttner 1999; Blom et al. 2006). In contrast to other cyanobacterial species, the filaments of P. * Corresponding author: posch@limnol.uzh.ch 1 Present address: Eawag, Department Aquatic Ecology, Dübendorf, Switzerland Limnol. Oceanogr., 56(1), 2011, 97–109 E 2011, by the American Society of Limnology and Oceanography, Inc. doi:10.4319/lo.2011.56.1.0097