Growth of heterotrophic aquatic bacteria in winter is controlled by organic matter availability rather than temperature

In winter 2009/10, a sudden under-ice bloom of heterotrophic bacteria occurred in the seasonally ice-covered, temperate, deep, oligotrophic Lake Stechlin (NE Germany). Extraordinary high bacterial abundance and biomass were fueled by the breakdown of a massive bloom of Aphanizomenon flos-aquae. The ice-cover was blanketed by snow leading to a significant reduction of the incident light. This exerted a pronounced physiological stress on the cyanobacteria. These were rapidly colonized by heterotrophic bacteria resulting in a sudden proliferation of associated and subsequently of free-living bacteria. Total bacterial protein production reached 201 µg C l-1 d-1 - ca. five times higher than previously measured values that year. Fluorescence in situ hybridization and denaturing gradient gel electrophoresis at high temporal resolution showed a sharp change in bacterial community structure coinciding with changes in cyanobacteria physiology. Pyrosequencing of 16S rRNA genes revealed that during cyanobacteria breakdown diversity of cyanobacteria-associated and free-living bacteria communities were reduced to a few dominant families. Some of these families were not detectable during the early stages of the cyanobacterial bloom indicating that senescent cells of cyanobacteria select for specific and well adapted bacterial communities. This massive bacterial bloom was rapidly terminated by heterotrophic nanoflagellates shortly before ice-off. Our case study suggests that in winter, unlike commonly postulated, carbon rather than temperature is the limiting factor for bacterial growth. This highlights the need for year-round studies of aquatic ecosystems including the winter season to correctly understand and model element and energy cycling through aquatic food webs, particularly the microbial loop.