Genetic Characterization of Periphyton Communities Associated with Selenium Bioconcentration and Trophic Transfer in a Simple Food Chain

Abstract

A major source of uncertainty in predicting selenium (Se) distribution in aquatic food webs lies in the enrichment factor (EF), the ratio of Se bioconcentration in primary producers and microorganisms relative to the concentration of Se in the surrounding water. It has been well demonstrated that EFs can vary dramatically among individual algal taxa, but data are lacking regarding the influence of periphyton community composition on EFs for a given geochemical form of Se. Therefore, the goals of this study were first to assess whether different periphyton communities could be established in aquaria with the same starting inoculum using different light and nutrient regimes, and second, to determine if the periphyton assemblage composition influences the uptake of waterborne Se (as selenite) and subsequent Se transfer to a model macroinvertebrate primary consumer. Periphyton biofilms were grown in aquaria containing filtered pond water (from Saskatoon, SK) spiked with approximately 20 μg Se/L (mean measured concentration 21.0 ± 1.2 μg Se/L), added as selenite. Five different light and nutrient regimes were applied to the aquaria (three replicates per treatment) to influence biofilm community development. After 6 weeks of biofilm maturation, 40 to 80 immature cultured snails (Stagnicola elodes) were added to each aquarium. The bacterial and algal members of the periphyton community were characterized by targeted metagenomic analyses before and after addition of snails to ensure the snails themselves did not significantly alter the biofilm community. Samples were collected for Se analysis of water, periphyton, and whole-body snail. The nutrient and light treatments resulted in substantially different compositions of the periphytic biofilms, with each being relatively consistent across replicates and throughout the study. Although the aqueous concentration of dissolved Se administered to treatments was constant, uptake by the different periphytic biofilms differed significantly. Both the low-light (61.8 ± 12.1 μg Se/g d.w.) and high-light (30.5 ± 4.7 μg Se/g d.w.) biofilms, which were found to have high proportions of cyanobacteria, contained statistically higher concentrations of Se relative to the other treatments. Furthermore, the concentration of Se in bulk periphyton was predictive of Se bioaccumulation in grazing snails but as an inverse relationship, opposite to expectations. The trophic transfer factor was inversely correlated with periphyton enrichment factor (r = -0.841). A number of different bacterial and algal taxa were correlated (either positively or negatively) with Se accumulation in periphyton biofilm and snails. Recent advancements in genetic methods make it possible to conduct detailed characterization of periphyton assemblages and begin to understand the influence that periphyton composition has on Se biodynamics in aquatic systems.

Application of autonomous sensor technology to estimate selenium exposure and a site‐specific selenium threshold in a Canadian boreal lake

“…Despite differences between years, Se enrichment in periphyton (Table 4) from both measured (2000-89 000 L/g) and sensor-estimated TSe (2670-55 500 L/g) are in the same order of magnitude reported in previous studies and also showed an inverse proportional relationship to TSe concentrations in water (Friesen et al, 2017;Markwart et al, 2019;Muscatello & Janz, 2009). Overall, the EF results suggest that without real-time data on estimated TSe concentrations, calculated EFs based on a few grab samples could underestimate time-integrated EFs at Sites 3, 4, and 6 in 2018 and Sites 6 and 10 in 2019.…”

Selenium Distribution and Trophic Transfer in the Periphyton–Benthic Macroinvertebrate Food Chain in Boreal Lakes Downstream from a Milling Operation

“…Chironomus dilutus and other Chironomidae species can reach Se equilibrium within 8 days of exposure (Franz et al, 2011), whereas pseudo–steady state took approximately 28 days in experiments with the amphipod H. azteca (Raes, 2020). A pseudo–steady state of 7 days was reported for the gastropod Stagnicola elodes , with slightly increasing Se concentrations over 21 days of exposure but not statistically different from day 7 (Friesen et al, 2017). Mayfly larvae (Heptageniidae) sampled from a mesocosms experiment seemed to have reached Se steady state before 21 days of exposure (Graves et al, 2021).…”

“…Still, the 2018 results might be related to other variables not investigated in the present study, such as potential temporal changes in the proportion of Se oxyanions (selenate vs. selenite) in treated diluted effluent and lake water (Gojkovic et al, 2015; Schiavon et al, 2017). In addition, factors such as the ionic competition between sulfate (Supporting Information, Tables S3 and S4) and selenate for Se uptake by periphyton (DeForest et al, 2017; Fournier et al, 2006, 2010; Ponton et al, 2020) along with potential differences in periphyton community composition among years (Chételat et al, 1999; Friesen et al, 2017; Markwart et al, 2019) could help explain the results found. In the following year, overall lower aqueous Se concentrations in McClean Lake east basin prevented saturation limits from being reached by periphyton, and Se bioconcentration was, therefore, considerably lower.…”

Chemotaxonomic responses of autotrophic periphyton communities to nutrient additions in pools of an intermittent stream

“…The majority of research on nutrient limitation in rivers and streams has focussed on measuring overall changes in autotrophic biomass via Chl‐ a and ash free dry mass (AFDM). Biochemical approaches such as pigment analysis (Tamm et al, 2015) and metagenomics (Bengtsson et al, 2018; Friesen et al, 2017) increasingly are being used to characterise the functional taxonomy of freshwater periphyton. Specifically, chemotaxonomy based on algal accessory pigments via high performance liquid chromatography (HPLC) is an alternative and straightforward method which is compatible with algal nutrient limitation experiments (Dalton et al, 2015).…”