Effects of Hydrophobic and Electrostatic Cell Surface Properties of Bacteria on Feeding Rates of Heterotrophic Nanoflagellates

Abstract

The influence of cell surface hydrophobicity and electrostatic charge of bacteria on grazing rates of three common species of interception-feeding nanoflagellates was examined. The hydrophobicity of bacteria isolated from freshwater plankton was assessed by using two different methods (bacterial adhesion to hydrocarbon and hydrophobic interaction chromatography). The electrostatic charge of the cell surface (measured as zeta potential) was analyzed by microelectrophoresis. Bacterial ingestion rates were determined by enumerating bacteria in food vacuoles by immunofluorescence labelling via strain-specific antibodies. Feeding rates varied about twofold for each flagellate species but showed no significant dependence on prey hydrophobicity or surface charge. Further evidence was provided by an experiment involving flagellate grazing on complex bacterial communities in a two-stage continuous culture system. The hydrophobicity values of bacteria that survived protozoan grazing were variable, but the bacteria did not tend to become more hydrophilic. We concluded that variability in bacterial cell hydrophobicity and variability in surface charge do not severely affect uptake rates of suspended bacteria or food selection by interception-feeding flagellates.Grazing by phagotrophic protists can be considered a major source of mortality for suspended bacteria in marine and freshwater systems. In particular, heterotrophic nanoflagellates, which feed mostly by direct interception of single bacterial cells, have been identified as the main consumers of planktonic bacteria (12,40,46). There is increasing interest in qualitative aspects of this important selective agent for bacterial communities, such as selective grazing and adaptation of bacteria to predation. Recent studies have revealed that grazing is an important force shaping the structure and composition of communities of planktonic bacteria (17,20,28,51). Bacterial cell size is one of the major phenotypic traits which influence the predator-prey relationship between bacteria and heterotrophic nanoflagellates. Grazing rates increase with bacterial size (15, 48) due to increased encounter rates (11). On the other hand, bacteria reach a predation refuge when they grow beyond a certain size as they become morphologically inedible for nanoflagellates (21,22). In field and laboratory studies it has been shown that size-related differences in predation vulnerability can result in shifts in bacterial species composition during enhanced protozoan grazing (28, 49).It has been speculated that properties of bacteria other than size might also be relevant for vulnerability to grazers (27). There is, however, little evidence of effects of other phenotypic traits, such as motility (14) or the chemical surface composition (26,31,35,45) of bacterial cells, on protist grazing rates. Studies of bacterial ingestion (phagocytosis) by phagocytes of mammalian immune systems have revealed that bacterial surface properties, especially hydrophobicity, strongly affect the contact probability an...

Marine bacterial community structure resilience to changes in protist predation under phytoplankton bloom conditions

“…The physiological state of bacterial cells has also been suggested as a key factor in grazing selectivity (Del Giorgio and Gasol, 2008), and preferential grazing of the more active cells within a community by protist grazers has been repeatedly observed (Del Giorgio et al, 1996;Pernthaler et al, 1997;Simek et al, 1997;Tadonléké et al, 2005;Sintes and Del Giorgio, 2014). This is probably related to the general positive relation between cell size and activity in marine bacteria (Gasol et al, 1995;Hahn and Höfle, 2001;Matz and Jürgens, 2001;Matz et al, 2002;Corno and Jürgens, 2006), suggesting that larger bacterioplankton cells are also usually the most active ones. Moreover, there could be a concentration-dependent component, where grazing might be different on abundant versus non-abundant populations .…”

Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp.

“…Twelve strains of bacteria exhibiting comparable cell sizes within the flagellate prey spectrum as well as a wide range of surface characteristics and swimming speeds were selected from a set of 41 isolates. They had been obtained from freshwater con-tinuous cultures featuring grazing and non-grazing conditions (Matz & Jürgens 2001). Stock preparations were stored at -70°C until further cultivation.…”

“…They raised the attractive issue that chemical surface properties of bacteria might matter in natural microbial predator-prey interactions in an analogous fashion (Jürgens & Güde 1994). However, recent experiments focusing on the role of a physicochemical mechanism (hydrophobicity) in flagellate feeding have not brought forth consistent results (Monger et al 1999, Matz & Jürgens 2001). This suggests either a non-uniform importance among protozoan species or some complex interference of other, more specific bacterial surface variables.…”

“…Since some evidence for a complex selection behavior in interception-feeding flagellates has been provided (e.g. Landry et al 1991, Jürgens & De Mott 1995, Boenigk et al 2001b, Matz & Jürgens 2001, it is assumed that bacterial properties may influence different steps in the process of food acquisition.…”

Grazing rates and functional diversity of uncultured heterotrophic flagellates

“…Second, each species might have different prey preferences, being adapted to consume a specific part of the bacterial assemblage. The most critical parameter to define the grazing vulnerability of a given bacteria is its cell size (González et al, 1990), but other factors such as cell viability (Landry et al, 1991), surface properties (Matz and Jü rgens, 2001), motility (Matz and Jü rgens, 2005), phylogenetic affiliation (Jezbera et al, 2005) or food quality (Shannon et al, 2007) have been also demonstrated. Finally, intrinsic physiological parameters like the functional response (relationship of grazing rates with prey concentration) or the growth efficiency (conversion of ingested food to biomass) might explain adaptations to specific environmental settings.…”