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.

Highlights

  • Faecal contamination of freshwater is traditionally assessed through the enumeration of faecal indicator bacteria (FIB) such as Escherichia coli

  • A clonal culture of D. pulex was maintained in the laboratory at 20 ̊C, grown in artificial Daphnia medium (ADaM) [36] and fed with Nannochloris atomus obtained from the National Center for Marine Algae and Microbiota (NCMA) during at least 6 months prior to the trials

  • Bacterivory by higher organisms such as Daphnia is a major driver of bacterioplankton abundance and composition in freshwater bodies and it has been extensively studied by limnologists and microbial ecologists on natural bacteria in ponds, lakes and reservoirs [18,19,20,40]

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Summary

Introduction

Faecal contamination of freshwater is traditionally assessed through the enumeration of faecal indicator bacteria (FIB) such as Escherichia coli. Considering the central role of E. coli in microbial water quality assessment, it is essential to understand its fate in aquatic habitats. Several studies have addressed the impact of protozooplankton communities of heterotrophic nanoflagellates (HNF) and ciliates on E. coli [10,11] because they are major consumers of bacterioplankton in aquatic ecosystems [12,13]. Cladocerans (or “water fleas”) regroup cosmopolitan communities of freshwater microcrustaceans that are important components of aquatic food webs [15]. Daphnia can affect the biomass of aquatic microbial communities and shape their size structure and species composition, either by direct consumption of bacteria or indirectly by predation on bacterivorous nanoflagellates and ciliates [19,20,21,22,23]

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