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 seasonspecific 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.

Microbial food webs in hypertrophic fishponds: Omnivorous ciliate taxa are major protistan bacterivores

“…Flagellate and ciliate bacterivory rates were estimated using FLB (Sherr and Sherr ) prepared from a mixture of isolated strains from the genus Limnohabitans and Polynucleobacter . The strains are typical and highly abundant members of bacterioplankton in lakes (Jezbera et al ) and were isolated from Římov reservoir: Limnohabitans planktonicus (short rods, MCV of 0.135 μ m 3 ) and Limnohabitans parvus (short rods, MCV of 0.055 μ m 3 , see Kasalický et al ) and one undescribed strain (czRimov8‐C6) was from the PnecC lineage of Polynucleobacter (short curved rods, MCV of 0.054 μ m 3 , Šimek et al ). The cells were harvested at early stationary phase and mixed at a similar numerical ratio that yielded MCV ± SD of the mixture cells of 0.072 ± 0.022 μ m 3 , which matched well the typical MCV of bacteria in the fishponds (0.075 ± 0.029 μ m 3 , median 0.066 μ m 3 ).…”

“…We also have a solid theoretical base for evaluating feeding preferences and functional responses of distinct pelagic protistan groups to various food resources (e.g., Montagnes et al 2008). However, most of our knowledge is derived from studies of cultured protistan species (Wickham 1995;Weisse et al 2016) and there is relatively little empirical evidence or direct quantification of the contribution of different protistan groups to in situ carbon flows (e.g., Sanders et al 1989;Gaedke et al 2002;Posch et al 2015;Šimek et al 2018). We also lack knowledge concerning how microbial food webs may vary in different systems.…”

Determining lineage-specific bacterial growth curves with a novel approach based on amplicon reads normalization using internal standard (ARNIS)

“…The growth rate can be directly determined in microbial cultures as the relative change of biomass (frequently approximated by microscopy counts) per unit of time [ 3 , 4 ]. Despite the fact that laboratory experiments provide invaluable information on bacterial growth and physiology [ 5 , 6 ], they cannot be directly applied in natural planktonic communities, where a fraction of the biomass is constantly removed at lineage-specific rates by protozoan grazing, viral lysis, or UV damage [ 7 , 8 ]. Therefore, in situ bacterial specific growth rates are typically determined using manipulation experiments, in which mortality is reduced using pre-filtration and/or dilution, and the growth is followed by microscopy [ 9 ].…”

“…The response of individual bacterial groups can be determined using fluorescence in situ hybridization (FISH) technique [ 10 ]. This approach has largely expanded our knowledge about the activity and ecology of the main bacterial groups [ 1 , 7 ]. However, this labor-intensive approach allows only for a handful of main phylotypes to be followed in a single study.…”

Microbial drama in four acts - Extreme rain events cause cyclic succession in plankton communities

“…Protozoan bacterivory was estimated using fluorescently labelled bacteria(FLB) prepared from a mixture of cultures of small rods of Limnohabitans lineage LimC44,53 and two undescribed strains of Polynucleobacter lineage PnecC. The sizes of FLB reassembled the typical size class distribution of the bacterioplankton in the pond.…”