A finely tuned symphony of factors modulates the microbial food web of a freshwater reservoir in spring

Abstract

We employed high frequency sampling to determine the major factors modulating microbial food-web composition and dynamics through the spring phytoplankton bloom and clear-water phases in a freshwater reservoir. We examined effects of a changing trophic structure of the planktonic community cascading from the level of zooplankton, through phytoplankton composition and exudation rates to the level of growth responses and losses to grazers of phylogenetically narrow bacterial lineages. Specific probes for fluorescence in situ hybridization (FISH) revealed important short-lived peaks of genus-like (Fluviiciola sp. and Limnohabitans spp.) or even taxonomically narrower populations of Betaproteobacteria and Flavobacteria (such as FlavB and Flav2 lineages). Protozoan grazing on bacterioplankton was studied by using fluorescently labeled bacteria and by direct analyses of FISH-probe-targeted bacterial phylotypes in flagellate food vacuoles. Evaluations of selective bacterivory, growth responses, and cell biovolumes of various bacterial groups during the spring bloom indicated that certain bacterial groups such as Limnohabitans can contribute to carbon flow to the grazer food chain up to 10-fold more than similarly abundant small cells from the Ac1 lineage of Actinobacteria. During the clear-water phase, filter-feeding cladocera had dominant effects on bacterioplankton abundance and community dynamics, likely through direct grazing on larger bacteria along with altering major substrate pools (via e.g., the herbivores' sloppy feeding on algae). Fine-temporal resolution data revealed several environmental scenarios, in which the interplay of distinct top-down and bottom-up factors resulted in a competitive advantage of particular bacterial lineages.

A population of giant tailed virus-like particles associated with heterotrophic flagellates in a lake-type reservoir

“…Azam et al 1983). In limnetic systems, population densities of flagellates are thought to be controlled by grazers, specifically larger protists such as ciliates, and larger zooplankton such as rotifers, copepods, and cladocerans (Jürgens et al 1997, Jürgens & Jeppesen 2000, Sommer et al 2012, Šimek et al 2014. During the last two and a half decades, a plethora of information has been accumulated on viruses controlling bacterioplankton (e.g.…”

Prey-Specific Growth Responses of Freshwater Flagellate Communities Induced by Morphologically Distinct Bacteria from the Genus Limnohabitans

“…This has also been suggested for several phylogenetically narrow lineages of Flavobacteria (6,7,9). Representatives of both the Flavobacteria and the Limnohabitans genera are dominated by larger cell sizes (9) yet are within the edible size range for HNF (26,27). Notably, it has been shown that the high growth rates of Limnohabitans bacteria are counterbalanced by considerable loss rates via grazing because these bacteria are selectively grazed by flagellates (9,28).…”

“…Thus, it seems that the main substrates supporting their rapid growth in situ are alga-derived substances (19,24,25). This has also been suggested for several phylogenetically narrow lineages of Flavobacteria (6,7,9). Representatives of both the Flavobacteria and the Limnohabitans genera are dominated by larger cell sizes (9) yet are within the edible size range for HNF (26,27).…”

“…Representatives of both the Flavobacteria and the Limnohabitans genera are dominated by larger cell sizes (9) yet are within the edible size range for HNF (26,27). Notably, it has been shown that the high growth rates of Limnohabitans bacteria are counterbalanced by considerable loss rates via grazing because these bacteria are selectively grazed by flagellates (9,28). It is because of these specific ecophysiological traits, high growth rate and high grazing pressure, that Limnohabitans bacteria likely have a prominent role in carbon transfer to higher trophic levels.…”

“…The amount, composition, and temporal dynamics of DOM differ widely among the diverse set of freshwater ecosystems, and this DOM distinctly modulates the growth and population dynamics of different bacterioplankton taxa (6). For instance, some bacterioplankton groups, such as Betaproteobacteria and Flavobacteria, can respond to sudden pulses in alga-derived organic carbon very rapidly, using doubling times (DTs) that vary from several hours to days (7)(8)(9)(10).…”