Bacterial prey food characteristics modulate community growth response of freshwater bacterivorous flagellates

Abstract

Different bacterioplankton species represent different food quality resources for heterotrophic nanoflagellate (HNF) communities, potentially affecting HNF growth, community dynamics and carbon flow to higher trophic levels. However, our knowledge of such dynamics is still very limited. Here, we describe the results of 11 experiments with natural HNF communities from distinct seasonal phases in two freshwater habitats. The HNF communities were released from predation pressure of zooplankton and incubated with 16 distinct ecologically relevant prey bacterial strains from important Betaproteobacteria genera (Limnohabitans, Polynucleobacter, and Methylopumilus) and one Actinobacteria strain from the Luna 2 cluster. We observed remarkable prey- and season-specific variability in community HNF growth parameters, i.e., doubling time, volumetric gross growth efficiency (GGE), and length of lag phase. All strains, except for the actinobacterium, supported rapid HNF population growth with an average doubling time of 10 h and GGE of 29%. Our analysis revealed that 59% of the variability in flagellate GGE data was explained by the length of lag phase after prey amendments. This indicates a considerable “adaptation time,” during which the predator communities undergo compositional shifts toward flagellate bacterivores best adapted to grow on the offered prey. Importantly, the rapid HNF growth detected on various bacteria tightly corresponds to doubling times reported for fast growing bacterioplankton groups. We propose a conceptual model explaining the tight linkages between rapid bacterial community shifts and succeeding HNF community shifts, which optimize prey utilization rates and carbon flow from various bacteria to the microbial food chain.