High motility reduces grazing mortality of planktonic bacteria

Abstract

We tested the impact of bacterial swimming speed on the survival of planktonic bacteria in the presence of protozoan grazers. Grazing experiments with three common bacterivorous nanoflagellates revealed low clearance rates for highly motile bacteria. High-resolution video microscopy demonstrated that the number of predator-prey contacts increased with bacterial swimming speed, but ingestion rates dropped at speeds of >25 microm s(-1) as a result of handling problems with highly motile cells. Comparative studies of a moderately motile strain (<25 microm s(-1)) and a highly motile strain (>45 microm s(-1)) further revealed changes in the bacterial swimming speed distribution due to speed-selective flagellate grazing. Better long-term survival of the highly motile strain was indicated by fourfold-higher bacterial numbers in the presence of grazing compared to the moderately motile strain. Putative constraints of maintaining high swimming speeds were tested at high growth rates and under starvation with the following results: (i) for two out of three strains increased growth rate resulted in larger and slower bacterial cells, and (ii) starved cells became smaller but maintained their swimming speeds. Combined data sets for bacterial swimming speed and cell size revealed highest grazing losses for moderately motile bacteria with a cell size between 0.2 and 0.4 microm(3). Grazing mortality was lowest for cells of >0.5 microm(3) and small, highly motile bacteria. Survival efficiencies of >95% for the ultramicrobacterial isolate CP-1 (< or =0.1 microm(3), >50 microm s(-1)) illustrated the combined protective action of small cell size and high motility. Our findings suggest that motility has an important adaptive function in the survival of planktonic bacteria during protozoan grazing.

FIG. 1.

Clearance rates of three flagellates on bacterial strains with different motility. P. pavonaceae KB6 showed mean swimming speeds of 17 μm s⁻¹, P. rhodesiae KB23 showed speeds of 29 μm s⁻¹, and P. aeruginosa SG81R1 showed speeds of 44 μm s⁻¹. Bacteria were sorted in the order of increasing swimming speed. Error bars indicate standard deviations of three replicates.

FIG. 2.

Interaction between Spumella sp. and moderately motile P. pavonaceae KB6 (a to c) and highly motile Acidovorax sp. strain CP-2 (d to f). After the prey bacterium is caught in the feeding current of the flagellate (a and d), the moderately motile KB6 is captured by the long flagellum of the flagellate (b) and forced into a food vacuole after 2.3 s (c). Note that the highly motile CP-2 escapes the capture reaction of the flagellate after cell contact (e) and moves out of reach within less than 0.5 s (f). The arrow indicates the location of the prey bacterium. Light video microscopy was used (1,200×, oil immersion). Bar = 5 μm.

FIG. 3.

Flagellate feeding and bacterial survival parameters at different bacterial swimming speeds. The upper graph (A) shows contact rates between bacteria and flagellates (○) and ingestion rates (•). The lower graph (B) illustrates bacterial escape efficiencies after contact with the flagellate (□) and total survival efficiencies (▪). Values are given as means ± standard deviations based on the evaluation of 12 replicates.

FIG. 4.

Grazing-mediated changes of the swimming speed distribution of moderately motile P. rhodesiae CP-17 and highly motile Acidovorax sp. strain CP-2. The top panels show speed distributions before the addition of the flagellate Ochromonas sp. The lower graphs show swimming speed distributions after 5 and 10 h of grazing. The dotted line indicates the median swimming speed. Values of each speed class are given as means ± standard deviations of three replicates. N gives the average number of bacterial cells counted by the motion analysis software.

FIG. 5.

Impact of growth rate and starvation on bacterial swimming speed and cell size. Three bacterial isolates (Acidovorax sp. strain CP-2, P. rhodesiae CP-17, and P. fluorescens CM10) were grown in continuous culture at two different growth rates (A), and culture subsamples were kept without nutrient supply for 20 days (B). The upper graph (A) shows the effect of a 10-fold increase in bacterial growth rate μ from 0.02 h⁻¹ (filled symbols) to 0.2 h⁻¹ (open symbols). The lower graph (B) illustrates changes of cultures which were grown at μ = 0.02 h⁻¹ (filled symbols) and starved for 20 days (open symbols). Values are given as means ± standard deviations on three consecutive days.

FIG. 6.

Bacterial survival efficiencies in the presence of grazing in relation to bacterial cell size and swimming speed. The data presented were pooled from this study and an earlier study which followed the same experimental design (20) to give a total of 23 data points. Each value is the mean of 12 individual observations of flagellate feeding behavior evaluated by high-resolution video microscopy.