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

Abstract

bBecause their large growth potential is counterbalanced with grazing by heterotrophic nanoflagellates (HNF), bacteria of the genus Limnohabitans, which are common in many freshwater habitats, represent a valuable model for examining bacterial carbon flow to the grazer food chain. We conducted experiments with natural HNF communities taken from two distinct habitats, the meso-eutrophic Ř ímov Reservoir and the oligo-mesotrophic Lake Cep (South Bohemia). HNF communities from each habitat at distinct seasonal phases, a late April algal bloom and a late May clear water phase, were each fed 3 Limnohabitans strains of differing cell sizes. Water samples were prefiltered (5 m) to release natural HNF communities from zooplankton control and then amended with the Limnohabitans strains L. planktonicus II-D5 (medium sized, rod shaped), Limnohabitans sp. strain T6-5 (thin, long, curved rod), and Limnohabitans sp. strain 2KL-3 (large solenoid). Using temporal sampling and prey treatment, we determined HNF growth parameters such as doubling time, growth efficiency, and length of lag phase prior starting to exponential growth. All three Limnohabitans strains supported HNF growth but in significant prey-, site-, and season-dependent fashions. For instance, addition of the moderately large T6-5 strain yielded very rapid HNF growth with a short lag phase. In contrast, the curved morphology and larger cell size of strain 2KL-3 made this prey somewhat protected against grazing by smaller HNF, resulting in slower HNF growth and longer lag phases. These trends were particularly pronounced during the late May clear-water phase, which was dominated by smaller HNF cells. This may indicate a longer "adaptation time" for the flagellate communities toward the large prey size offered.T he importance of both bacteria and their protistan grazers in planktonic microbial food webs has been widely recognized (1, 2). Bacterioplankton transfers dissolved organic matter (DOM) to bacterial biomass that is consumed mainly by heterotrophic nanoflagellates (HNF) or ciliates and channeled via grazing into the metazoan grazer food chain (3-5). 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 (7-10).Representatives from a few highly abundant phylogenetic clusters of Betaproteobacteria and Actinobacteria frequently dominate bacterioplankton populations in a wide variety of freshwater ecosystems (11-13). Among the Betaproteobacteria, Limnohabitans and Polynucleobacter have been documented as the most ecologically important genera (6,(14)(15)(16)(17)(18). The Limnohabitans genus is composed of five major lineages. Four are the so-called R-BT bacteria, which are...

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

“…We examined the growth potential and biomass transfer efficiency of natural HNF communities feeding on a very broad spectrum of relevant planktonic bacterial groups so far not employed in previous investigations (cf. Šimek et al 2013; Grujčić et al ; Weisse et al ). Moreover, our study has brought new insights into food quality aspects of the prey bacteria and revealed both general and prey‐specific trends in the growth responses of natural HNF communities to changing prey food quality represented by 16 distinct bacterial strains (Figs.…”

“…) related to different temporal community dynamics of bacterivorous HNF that have been previously described (e.g., Šimek et al ; Domaizon et al ; Nolte et al ). However, the responses of the natural grazer communities to enrichment with particular prey over different plankton successional phases have rarely been demonstrated (Grujčić et al ). Additionally, comparisons of the same prey amendments in samples from the reservoir and the lake revealed significant differences in HNF growth parameters that can be related to different seasonal succession of plankton and different trophic status of the lakes (experiments III–VI, for a detailed analysis see also Grujčić et al ).…”

“…During the exponential growth phase, bacterial cells (50 mL) were concentrated by centrifugation at 5000 × g and subsequently re‐suspended into 50 mL of 0.2‐μm filtered and sterilized water from the Římov Reservoir (experiments I–III, V, and VII–XI, see Table ), or water from Lake Cep (experiments IV and VI). The cultures were kept on a shaker overnight to facilitate even re‐suspension of cells and adaptation to the reservoir or lake water as detailed elsewhere (Šimek et al 2013; Grujčić et al ). Ca .…”

“…Many different methods to study HNF bacterivory have been proposed; however, none are appropriate for assessing the specific role of a naturally abundant prey in carbon flow dynamics (Montagnes et al ). So far only a few experimental studies have focused on the growth responses of natural HNF assemblages to bacterial prey amendments using strains of relevant prokaryotic taxa that are those originating from the same systems as the consumers (Šimek et al 2013; Grujčić et al ). The lack of such data severely limits the possibility to generalize preliminary evidence on a tight coupling between prey community shifts and variable growth responses of HNF associated with very rapid shifts in the grazer community (Šimek et al 2013), the phenomena that can be modulated by seasonally evolving trophic structure of plankton environments (e.g., Grujčić et al ).…”

“…Different bacterial strains appear to have different nutritional value to consumers (Boenigk et al 2006;Tarao et al 2009;Simek et al 2013;Chrzanowski and Foster 2014) and this characteristic may vary even for the same prey during different seasonal phases within the same ecosystems (Grujčić et al 2015). Moreover, the same bacterial species may not have similar nutritional quality for all members of the flagellate community (Chrzanowski and Foster 2014).…”