Microbial Food Webs in Boreal Humic Lakes and Reservoirs: Ciliates as a Major Factor Related to the Dynamics of the Most Active Bacteria

Abstract

In order to assess the factors that determine the dynamics of bacteria with high nucleic acid content in aquatic systems, we (i) conducted 24-h in situ dialysis experiments, involving different fractions of plankton and unfiltered water and (ii) examined empirical relationships between bacteria and both abiotic factors and protists, in boreal humic freshwaters (reservoir and lakes) in the James Bay region (Québec, Canada). Bacteria were subdivided into two subgroups on the basis of their nucleic acid content assessed by flow cytometry. The abundance of bacteria with the highest nucleic acid content and high light scatter (HNA-hs) was significantly correlated, across sites, to bacterial production, whereas bacteria with lower nucleic acid content (LNA) and total bacteria were not. In addition, HNA-hs growth was higher and more variable than LNA growth, indicating that HNA-hs were the most dynamic bacteria. Heterotrophic nanoflagellate and ciliate biomass represented, on average, 5 and 13% of bacterial biomass, respectively. Both in ambient waters and in experiments, ciliates were significantly and negatively correlated with bacteria, whereas heterotrophic nanoflagellates, likely under the grazing pressure from ciliates and metazooplankton, were not. Among ciliates, Cyclidium glaucoma appeared to play an important role. Its growth was significantly and negatively correlated to that of HNA-hs but not to that of LNA. In ambient waters, the abundance of this species explained 56% of the variations in HNA-hs abundance and only 27% of those for LNA. The abundances of total bacteria and LNA significantly increased with chlorophyll a, whereas those of HNA-hs did not. In addition, during the experiments, the estimated potential losses of HNA-hs significantly increased with the initial abundance of C. glaucoma. These results suggest selective removal of the most dynamic bacteria by C. glaucoma and indicate that ciliates may play an important role in the dynamics of active bacteria in natural waters. These findings suggest the existence, within the aquatic microbial food webs, of keystone species that are very important in regulating the activity structure of bacteria.