Grazing of heterotrophic flagellates on viruses is driven by feeding behaviour

Abstract

The trophic interactions between viruses, bacteria and protists play a crucial role in structuring microbial communities and regulating nutrient and organic matter flux. Here, we show that the impact on viral density by heterotrophic flagellates is related to their feeding behaviour (feeding on sedimented particles - Thaumatomonas coloniensis, filter feeding of suspended particles - Salpingoeca sp., and actively searching raptorial feeding - Goniomonas truncata). Phage MS2 was co-incubated with flagellates and the natural bacterial and viral community originating from the same groundwater habitats where the flagellates were isolated. Three complementary assays, i.e. flow cytometry, qPCR and plaque assay, were used for enumeration of total viruses, total MS2 phages, and free and infectious MS2, respectively, to provide insights into the grazing mechanisms of the flagellates on viruses. Phage MS2 was actively removed by the suspension feeders T. coloniensis and Salpingoeca sp. in contrast with the actively raptoriale grazer G. truncata. The decline of viral titre was demonstrated to be caused by ingestion rather than random absorption by both qPCR and locating protein fluorescently labelled MS2 inside the flagellates. Further, we indicate that phages can be used as a minor carbon source for flagellates. Collectively, these data demonstrate that eliminating viruses can be an important function of protists in microbial food webs, carbon cycling and potentially water quality control.

A Generalist Protist Predator Enables Coexistence in Multitrophic Predator-Prey Systems Containing a Phage and the Bacterial Predator Bdellovibrio

“…BALO and phage growth, however, significantly decreased in the presence of the protist (Figures 3d,e) and also in the case of BALO when both protist and phage were present (Figure 3b). This indicates that the protist either ingested free BALOs (Johnke et al, 2017), phages (Deng et al, 2014), or BALO-or phage-infected prey, or was the strongest resource competitor. Another possibility is an indirect effect of the overall prey density reduction by protist predation, which might have substantially lowered the resource availability for the BALO and phage and consequently reduced the growth of the latter.…”

“…Direct (straight) and indirect (dashed) interactions exist between all predators. Direct predatory interactions are known for protists and BALOs (Johnke et al, 2017); and protists and phages (Deng et al, 2014). Additionally, superinfection of a prey bacterium by a BALO and a phage was shown by 1992) prior to the experiments.…”

“…Depending upon their feeding strategies, protists may indirectly remove phages by lowering the susceptibility of the shared prey to phages (Deng et al, 2014;Ormala-Odegrip et al, 2015). However, detailed information on the impact of micro-predator interactions on microbial communities is missing (Johnke et al, 2014).…”

Prediction of fecal indicator organism concentrations in rivers: the shifting role of environmental factors under varying flow conditions

“…Grazing is size selective [43] and most protists graze preferentially on medium-sized bacterial cells [44]. Although there is evidence that some flagellates are able to feed on phages and viruses [45], they are likely grazed on to a lesser extent than bacteria and can, therefore, be described more precisely by hydrological and meteorological factors. This is further supported by the calculated relative differences between viral and bacterial FIO (Additional file 1: Figure S3 Conclusively, grazing instead of pH is most likely responsible for the loss of fecal bacteria in the Moselle based on the higher secondary productivity.…”

Effects of cell morphology and attachment to a surface on the hydrodynamic performance of unicellular choanoflagellates

“…Protozoans play an important role in aquatic food webs and the carbon cycle [1][2][3][4][5]. Choanoflagellates, flagellated eukaryotes that are abundant in marine and freshwater habitats, are important predators on bacteria in aquatic ecosystems [6][7][8]. Not only are choanoflagellates important ecologically, but they are also of evolutionary interest, because they are the closest living relatives of the animals [9].…”