Distinctive patterns in prokaryotic community composition in response to viral lysis and flagellate grazing in freshwater microcosms

Abstract

Summary We conducted microcosm experiments to examine the effect of viruses and heterotrophic nanoflagellates (together referred to as top‐down factors) on prokaryotic standing stock and prokaryotic community composition during the clear water phase (autumn season) in the oligotrophic Lake Pavin in France. In the experimental treatments containing viruses and viruses plus flagellates, the dissolved organic matter released through top‐down activity appeared to stimulate prokaryotic biomass production and viral proliferation. About 68% of the total prokaryotic abundance detected by fluorescence in situ hybridization (FISH) revealed the dominance of typical freshwater groups, which included Beta‐proteobacteria, Actinobacteria and Cytophaga‐Flavobacterium subgroups at the start of the experiments. The manipulation of viruses and flagellates (presence or absence) was successful in inducing significant changes in prokaryotic community composition at a broad phylogenetic level, suggesting that prokaryotic lifestyles are influenced by top‐down factors. The Beta‐proteobacteria subgroup, which outgrew other prokaryotic groups in the absence of viruses and flagellates, was strongly suppressed and vulnerable to mortality in the presence of both the factors. Alpha‐proteobacteria and Actinobacteria subgroups grew significantly in the presence of top‐down factors, suggesting that the dissolved organic matter (regenerated nutrients) released through their activity favoured the development of these groups. The Cytophaga‐Flavobacterium subgroup failed to show any functional response in the presence or absence of top‐down factors. Low prokaryotic diversity in the experimental treatment containing viruses and high diversity in the presence of both top‐down factors were observed. We found synergistic interactions in treatments when both top‐down factors were present, suggesting that the process of nutrient regeneration was crucial in sustaining stable prokaryotic communities.