Strain-specific differences in the grazing sensitivities of closely related ultramicrobacteria affiliated with the Polynucleobacter cluster

Abstract

Ultramicrobacteria (cell volume < 0.1 microm(3)) are the numerically dominant organisms in the plankton of marine and freshwater habitats. Flagellates and other protists are assumed to be the most important predators of these ultramicrobacteria as well as of larger planktonic bacteria. However, due to controversial observations conducted previously, it is not clear as to whether fractions of the ultramicrobacteria are resistant to flagellate predation. Furthermore, it is not known if closely related bacteria vary significantly in their sensitivity to flagellate predation. We investigated the sensitivity of ultramicrobacteria affiliated with the cosmopolitan Polynucleobacter cluster to grazing by Spumella-like nanoflagellates. Laboratory grazing experiments with four closely related (> or =99.6% 16S rRNA gene sequence similarity) bacteria and three closely related (100% 18S rRNA gene sequence similarity) flagellates were performed. In comparison to larger bacteria, predation on the ultramicrobacterial Polynucleobacter strains was weak, and the growth of the predating flagellates was slow. Specific clearance rates ranged between 0.14 x 10(5) and 2.8 x 10(5) units of predator size h(-1). Feeding rates strongly depended on the flagellate and bacterial strain (P < 0.001). Grazing mortality rates of the three flagellate strains investigated varied for the same prey strain by up to almost fourfold. We conclude that (i) ultramicrobacteria affiliated with the Polynucleobacter cluster are not protected from grazing, (ii) strain-specific variations in grazing sensitivity even between closely related bacteria are high, and (iii) strain-specific differences in predator-prey interaction could be an important factor in the evolution and maintenance of microbial microdiversity.

FIG. 1.

Grazing mortality rates of the Spumella-like flagellates grazing on four strains of ultramicrobacteria affiliated with the Polynucleobacter cluster.

FIG. 2.

Abundance of bacterial strains, at the start (0 h; black bars) as well as the end (158 h; grey bars) of the long-term grazing experiment with flagellate strains JBC07 and JBNZ41. Towards the end of the experiment, flagellate abundances were already decreasing. This indicates that the flagellates were not able to graze the bacteria below 0.8 × 10⁶ to 2.2 × 10⁶ bacteria ml⁻¹ and that grazing at these bacterial concentrations did not even support the basic metabolic costs of maintaining the flagellate population.

FIG. 3.

Specific clearance versus predator-prey size ratio based on volume. Flagellate strains are represented by the large black symbols: JBC07 (pentagon), JBM10 (circle), JBNZ41 (square), and Ochromonas sp. strain DS (diamond). Bacterial strains are represented by small white symbols: MWH-NR1 (triangle), MWH-TaW3 (+), MWH-MoIso2 (circle), MWH-VicM1 (square), and B. diminuta (upside-down triangle).