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

Abstract

The fecal indicator bacterial species Escherichia coli is an important measure of water quality and a leading cause of impaired surface waters. We investigated the impact of the filter-feeding metazooplankton Daphnia magna on the inactivation of E. coli. The E. coli clearance rates of these daphnids were calculated from a series of batch experiments conducted under variable environmental conditions. Batch system experiments of 24 to 48 h in duration were completed to test the impacts of bacterial concentration, organism density, temperature, and water type. The maximum clearance rate for adult D. magna organisms was 2 ml h−1 organism−1. Less than 5% of E. coli removed from water by daphnids was recoverable from excretions. Sorption of E. coli on daphnid carapaces was not observed. As a comparison, the clearance rates of the freshwater rotifer Branchionus calyciflorus were also calculated for select conditions. The maximum clearance rate for B. calyciflorus was 6 × 10−4 ml h−1 organism−1. This research furthers our understanding of the impacts of metazooplankton predation on E. coli inactivation and the effects of environmental variables on filter feeding. Based on our results, metazooplankton can play an important role in the reduction of E. coli in natural treatment systems under environmentally relevant conditions. IMPORTANCE Escherichia coli is a fecal indicator bacterial species monitored by the U.S. Environmental Protection Agency to assess microbial water quality. Due to the potential human health implications linked to high levels of E. coli, it is important to understand the inactivation or reduction mechanisms in surface waters. Our research examines the capacities of two types of widespread filter-feeding freshwater metazooplankton, Daphnia magna and Brachionus calyciflorus, to reduce E. coli concentrations. We examine the impacts of different environmentally relevant conditions on the clearance rates. Our results contribute to a better understanding of the importance of metazooplankton in controlling E. coli concentrations and what conditions will reduce or increase grazing. These results provide baseline data to support future efforts to develop a quantitative model relating zooplankton uptake rates to relevant environmental variables.

Zooplankton as a transitional host forEscherichia coliin freshwater

“…In this study we found that Daphnia can function as a short-term and transitional host for E. coli: as hypothesised, Daphnia did reduce abundances of E. coli in the surrounding waters but it was not responsible for the complete removal of E. coli, since many bacterial cells survived gut passages (Figure 5) and E. coli was still detected after 10 days of co-culturing with Daphnia (Figures 5 and 6). In this study we confirm that E. coli localizes mainly in the gut of Daphnia and that at least part of its population survives the gut passage (Burnet, et al 2017;Ismail, et al 2019). However, the association with Daphnia obtusa did not seem to give a long term advantage in the survival of E. coli (Figures 6&7).…”

“…Many studies have recently suggested to use Daphnia as a biological controlling mechanism for E. coli contaminations in water: through experiments using very large densities of animals and bacteria these studies showed that the abundance of E. coli was reduced due to grazing of Daphnia (Nørgaard and Roslev 2016;Burnet, et al 2017;Ismail, et al 2019). The addition of Daphnia is surely feasible to reduce large abundances of E. coli, but here we showed that E. coli persisted even in the presence of Daphnia in low abundances that were more similar to those found in nature.…”

“…It is generally assumed that the presence of Daphnia sp. reduces E. coli abundance in the water (Burnet, et al 2017;Ismail, et al 2019). Nevertheless, in a study based on 16S rRNA gene amplicon sequencing from a lake E. coli/Shigella made up for a large percentage of the copepod and Daphnia microbiota, but was present only with low abundances on stones, water and sediments ).…”

Zooplankton as a Transitional Host forEscherichia coliin Freshwater

“…It is generally assumed that the presence of Daphnia sp. reduces E. coli abundance in the water ( 37 , 38 ). Nevertheless, in a study based on 16S rRNA gene amplicon sequencing from a lake, E. coli /Shigella made up a large percentage of the copepod and Daphnia microbiota, but were present only at low abundance on stones, in water, and in sediments ( 39 ).…”

Water Chemistry, Exposure Routes, and Metal Forms Determine the Bioaccumulation Dynamics of Silver (Ionic and Nanoparticulate) in Daphnia magna

“…Filter-feeding zooplankton, such as daphnids, are abundant in natural treatment systems; they are a critical link in aquatic food chains and can significantly improve water quality through grazing (Fayer et al, 2000; This article contains online-only Supporting Information. Ismail et al, 2019;Jürgens et al, 1997;Shiny et al, 2005;Trout et al, 2002). Adverse effects of AgNPs on daphnids at environmentally relevant conditions could impact the efficacy of treatment wetlands.…”