Quantification of microcystin production and biodegradation rates in the western basin of Lake Erie

Abstract

Cyanobacterial biomass forecasts currently cannot predict the concentrations of microcystin, one of the most ubiquitous cyanotoxins that threaten human and wildlife health globally. Mechanistic insights into how microcystin production and biodegradation by heterotrophic bacteria change spatially and throughout the bloom season can aid in toxin concentration forecasts. We quantified microcystin production and biodegradation during two growth seasons in two western Lake Erie sites with different physicochemical properties commonly plagued by summer Microcystis blooms. Microcystin production rates were greater with elevated nutrients than under ambient conditions and were highest nearshore during the initial phases of the bloom, and production rates were lower in later bloom phases. We examined biodegradation rates of the most common and toxic microcystin by adding extracellular stable isotopelabeled microcystin-LR (1 μg L À1 ), which remained stable in the abiotic treatment (without bacteria) with minimal adsorption onto sediment, but strongly decreased in all unaltered biotic treatments, suggesting biodegradation. Greatest biodegradation rates (highest of À8.76 d À1 , equivalent to the removal of 99.98% in 18 h) were observed during peak bloom conditions, while lower rates were observed with lower cyanobacteria biomass. Cell-specific nitrogen incorporation from microcystin-LR by nanoscale imaging mass spectrometry showed that a small percentage of the heterotrophic bacterial community actively degraded microcystin-LR. Microcystin production and biodegradation rates, combined with the microcystin incorporation by single cells, suggest that microcystin predictive models could be improved by incorporating toxin production and biodegradation rates, which are influenced by cyanobacterial bloom stage (early vs. late bloom), nutrient availability, and bacterial community composition.

Microcystin Concentrations, Partitioning, and Structural Composition during Active Growth and Decline: A Laboratory Study

“…The stimulation of additional growth, which was indicated by changes in chl-a in several of the experiments, did not link to shifts in pMC levels except for short-lived, small increases in IR and CP. In line with the findings from other MC production studies, cellular resources may have been diverted away from MC production and toward growth due to limiting conditions further explaining a lack of pMC production during later time points [32].…”

“…Finally, the importance of potential MC-degrading bacteria as proxies for bloom stage and toxicity have been discussed previously in relation to pMC release [ 26 , 32 , 36 ]. While no community data were collected to characterize any shifts in the assemblages during the incubation trials, the initial characterization of the bloom-associated bacteria using high-throughput sequencing highlighted different relative contributions from taxa that have been associated with MC degradation and also indicated that Microcystis was the dominant toxin-producing genus upon bloom collections [ 37 ].…”

“…Dissolved MC remained above safe drinking-water thresholds (1 µg L −1 [ 17 ]) up to 100 days after the start of the experiment and was thus persistent, which was in agreement with lake studies that determined shorter pMC than dMC half-lives ( Table 4 ) [ 24 , 30 ]. While dMC has been detected following a bloom for lengthy time periods, experiments utilizing added MC spike-ins to natural assemblages found that the bacterial degradation of dMC-LR and dMC-RR resulted in differing, congener-specific half-life estimates of 0.06–8.3 and 1.1 ± 0.23 days, respectively ( Table 4 ) [ 32 , 43 ]. Spiking lake water with dMC and following bacterial degradation indicated that congeners MC-LR and MC-LF also differ in their persistence [ 26 ].…”

Microcystin congeners in Lake Erie follow the seasonal pattern of nitrogen availability

“…These two sites were selected for experimentation due to differing water quality, but both being prone to cyanobacterial blooms. Complete methods for these experiments are presented in Chaffin et al (2022) . Briefly, there were four nutrient enrichment treatments: (1) no enrichment control, (2) phosphate and nitrate, (3) phosphate and ammonium, and (4) phosphate and urea.…”

A novel cyanolytic bacterium, Pseudomonas fluorescens BG‐E as a potential biological control agent for freshwater bloom‐forming cyanobacteria Pseudanabaena spp.

“…Additionally, some of these cyanolytic bacteria have the potential to degrade cyanotoxins such as MCs and suppress blooms instantaneously (Li et al, 2016). Consequently, considerable attention has been paid to heterotrophic bacteria in freshwater due to their potential as agents to control or terminate the excessive growth of cyanobacteria (Van Le et al, 2022; Wang et al, 2020; Zhang et al, 2019) and to degrade cyanotoxins (Chaffin et al, 2022; Idroos & Manage, 2018; Nájera et al, 2017). Although the identification of an effective biological control agent is challenging, recognizing and isolating bacteria with the ability to lyse Microcystis sp.…”