Selective grazing by protists upon enteric bacteria in an aquatic system

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Abstract

It is well known that protozoan grazing can be an important agent of mortality for suspended bacteria, both in marine and freshwater environments. Considering that the presence of fecal contamination is a frequent phenomenon in tríese environments, and that Escherichia coli and the genus Enterococcus are indicators of microbiological water quality, the effect of protozoan grazing on E. coli and Enterococcus faecalis in Los Padres Lagoon waters (Buenos Aires, Argentina, 37° 56'30" S, 57° 44'30" W) was herein analyzed. Microcosm assays were carried out, simulating lacustrine conditions, confronting suspensions of autochthonous bacterivorous protozoans with suspensions of autochthonous and collection strains of E. coli and E. faecalis, combined and individually. Daily counts were made for evaluating bacterial survival and the number of ciliates. The results obtained indicate that there is a preferential sequence for bacterial removal in the water, where E. faecalis is more grazing-resistant than E. coli. Moreover, it was noted that the origin of bacterial strains influenced their sensitivity for grazing, at least in the short term (e.g. the collection strains were less affected). We conclude that protozoan grazing can modify the relative abundance of fecal indicator microorganisms, thus altering the results of water quality studies.

Translated abstract

Está bien establecido que la predación por protozoos puede ser un factor importante de mortalidad para las bacterias en suspensión, tanto en ambientes marinos como de agua dulce. Considerando que la contaminación fecal es un fenómeno frecuentemente observado en estos ambientes, y que Escherichia coli y miembros del género Enterococcus son indicadores de calidad microbiológica del agua, se analizó el efecto de la predación por protozoos sobre E. coli y Enterococcus faecalis en aguas de la Laguna de los Padres (Buenos Aires, Argentina, 37° 56'30" S, 57° 44'30" W). Se realizaron ensayos a microcosmos, simulando el ambiente lagunar, enfrentando suspensiones de protozoos bacterívoros autóctonos con suspensiones de cepas autóctonas y de colección de E. coli y E. faecalis, en forma individual y combinada. Diariamente se efectuaron los recuentos correspondientes para elaborar las curvas de supervivencia. Los resultados obtenidos indican que existe una secuencia en la eliminación de cepas bacterianas por bacterivoría, siendo E. faecalis más resistente a la predación que E. coli. Además, se observó que el origen de las cepas condiciona su sensibilidad a la predación, ya que las cepas provenientes de los cultivos de colección resultaron menos afectadas. Se concluye que la bacterivoría por protozoos puede modificar la abundancia relativa de los microorganismos indicadores de contaminación y, por ende, los resultados de los estudios de calidad del agua.

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Most cited references 12

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Off the hook--how bacteria survive protozoan grazing.

Carsten Matz, Staffan Kjelleberg (2005)

Bacterial growth and survival in numerous environments are constrained by the action of bacteria-consuming protozoa. Recent findings suggest that bacterial adaptations against protozoan predation might have a significant role in bacterial persistence and diversification. We argue that selective predation has given rise to diverse routes of bacterial defense, including adaptive mechanisms in bacterial biofilms, and has promoted major transitions in bacterial evolution, such as multicellularity and pathogenesis. We propose that studying predation-driven adaptations will provide an exciting frontier for microbial ecology and evolution at the interface of prokaryotes and eukaryotes.

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Grazing of protozoa and its effect on populations of aquatic bacteria.

Margaret Hahn, M Hofle (2001)

Predation by bacterivorous protists in aquatic habitats can influence the morphological structure, taxonomic composition and physiological status of bacterial communities. The protistan grazing can result in bacterial responses at the community and the species level. At the community level, grazing-induced morphological shifts have been observed, which were directed towards either larger or smaller bacterial sizes or in both directions. Morphological changes have been accompanied by changes in taxonomic community structure and bacterial activity. Responses at the species level vary from species to species. Some taxa have shown a pronounced morphological plasticity and demonstrated complete or partial shifts in size distribution to larger growth forms (filaments, microcolonies). However, other taxa with weak plasticity have shown no ability to reduce grazing mortality through changes in size. The impact of protistan grazing on bacterial communities is based on the complex interplay of several parameters. These include grazing selectivity (by size and other features), differences in sensitivity of bacterial species to grazing, differences in responses of single bacterial populations to grazing (size and physiology), as well as the direct and indirect influence of grazing on bacterial growth conditions (substrate supply) and bacterial competition (elimination of competitors).

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High motility reduces grazing mortality of planktonic bacteria.

Carsten Matz, Klaus Jürgens (2005)

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 ( 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 ( 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.