How does the cladoceran Daphnia pulex affect the fate of Escherichia coli in water?

Abstract

The faecal indicator Escherichia coli plays a central role in water quality assessment and monitoring. It is therefore essential to understand its fate under various environmental constraints such as predation by bacterivorous zooplankton. Whereas most studies have examined how protozooplankton communities (heterotrophic nanoflagellates and ciliates) affect the fate of E. coli in water, the capacity of metazooplankton to control the faecal indicator remains poorly understood. In this study, we investigated how the common filter-feeding cladoceran, Daphnia pulex, affects the fate of E. coli under different experimental conditions. Daphnia ingested E. coli and increased its loss rates in water, but the latter rates decreased from 1.65 d-1 to 0.62 d-1 after a 1,000-fold reduction in E. coli initial concentrations, due to lower probability of encounter between Daphnia and E. coli. The combined use of culture and PMA qPCR (viability-qPCR) demonstrated that exposure to Daphnia did not result into the formation of viable but non-culturable E. coli cells. In lake water, a significant part of E. coli population loss was associated with matrix-related factors, most likely due to predation by other bacterivorous biota and/or bacterial competition. However, when exposing E. coli to a D. pulex gradient (from 0 to 65 ind.L-1), we observed an increasing impact of Daphnia on E. coli loss rates, which reached 0.47 d-1 in presence of 65 ind.L-1. Our results suggest that the filter-feeder can exert a non-negligible predation pressure on E. coli, especially during seasonal Daphnia population peaks. Similar trials using other Daphnia species as well as stressed E. coli cells will increase our knowledge on the capacity of this widespread zooplankter to control E. coli in freshwater resources. Based on our results, we strongly advocate the use of natural matrices to study these biotic interactions in order to avoid overestimation of Daphnia impact.

Impact of Metazooplankton Filter Feeding on Escherichia coli under Variable Environmental Conditions

“…These approaches with chemically altered bacteria or beads may impact the feeding rate and do not consider inactivation, which is important when considering water quality implications. A recent study investigated the impact of bacterial concentration and daphnid density on the ingestion and inactivation of E. coli by Daphnia pulex using culture-based techniques (10). The observed trends and calculated uptake rates were different than those observed herein and could not be directly compared due to the different methodology and species used.…”

“…In addition, the lack of particles may result in reduced filtration rates, since fewer particles are encountered during grazing. Previous studies examining DAPI (4=,6-diamidino-2-phenylindole)-labeled E. coli cells fed to D. pulex showed that E. coli was contained within the food boluses of D. pulex, and uptake was observed within minutes of exposure (10). These studies also showed passage of E. coli cells within the gut, but DAPI stain could not be used to indicate viability (10).…”

“…Pond water filtered through a sterile 50-m sieve was spiked with E. coli K-12 to test whether clearance rates of bacteria were impacted when other food sources were available to the daphnids and E. coli only represented a fraction of the particulate matter. Including other particulate matter represents more realistic conditions for feeding studies (8,10). E. coli K-12 was inactivated at a significantly lower rate in pond water (0.56 Ϯ 0.1 ml h Ϫ1 daphnid Ϫ1 ) than in synthetic freshwater (1.4 Ϯ 0.1 ml h Ϫ1 daphnid Ϫ1 ) (P Ͻ 0.001) ( Fig.…”

“…When seasonal population density peaks, natural zooplankton communities have the ability to filter all the water in a lake within a 24-h time period (4)(5)(6). Zooplankton are often abundant in natural treatment systems and can filter feed on particles of various size ranges, including bacteria (7)(8)(9)(10). The contributions of zooplankton filter feeding to bacterial inactivation under variable environmental conditions are not well studied, and the viability of microbial pollutants after ingestion is uncertain.…”

Autonomous online measurement of β-D-glucuronidase activity in surface water: is it suitable for rapid E. coli monitoring?

“…S2). Standard curves were constructed using genomic DNA from a pure culture of E. coli (~10 7 CFU mL À1 ) as described earlier (Burnet et al, 2017). Genomic DNA was then serially log-diluted in DNase-free water.…”