Dataset Information

Isolation and Characterization of Lake Erie Bacteria that Degrade the Cyanobacterial Microcystin Toxin MC-LR.

ABSTRACT: Microcystin-LR (MC-LR) is a cyclic hepatotoxin produced by cyanobacteria, including Microcystis sp. and Planktothrix sp. Harmful algal blooms (HABs) in Lake Erie have become a major human health concern in recent years, highlighted by the August 2014 city of Toledo, Ohio, municipal water "do not drink" order that affected nearly 500,000 residents for 3 days. Given that microcystin degrading bacteria have been reported from HAB-affected waters around the world, we hypothesized that MC-LR degrading bacteria could be isolated from Lake Erie. To test this hypothesis, 13 water samples were collected from various Lake Erie locations during the summers of 2014 and 2015, MC-LR was continuously added to each water sample for 3 to 5 weeks to enrich for MC-LR-degrading bacteria, and MC-LR was quantitated over time. Whereas MC-LR was relatively stable in sterile-filtered lake water, robust MC-LR degradation (up to 19 ppb/day) was observed in some water samples. Following the MC-LR selection process, 67 individual bacterial isolates were isolated from MC-LR degrading water samples and genotyped to exclude potential human pathogens, and MC-LR degradation by smaller groups of bacterial isolates (e.g., groups of 22 isolates, groups of 11 isolates, etc.) was examined. Of those smaller groups, selected groups of four to five bacterial isolates were found to degrade MC-LR into non-toxic forms and form robust biofilms on siliconized glass tubes. Taken together, these studies support the potential use of isolated bacterial isolates to remove MC-LR from drinking water.

SUBMITTER: Thees A

PROVIDER: S-EPMC7402192 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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Isolation and Characterization of Lake Erie Bacteria that Degrade the Cyanobacterial Microcystin Toxin MC-LR.

Thees Alison A Atari Ealla E Birbeck Johnna J Westrick Judy A JA Huntley Jason F JF

Journal of Great Lakes research 20181116 1

Microcystin-LR (MC-LR) is a cyclic hepatotoxin produced by cyanobacteria, including <i>Microcystis</i> sp. and <i>Planktothrix</i> sp. Harmful algal blooms (HABs) in Lake Erie have become a major human health concern in recent years, highlighted by the August 2014 city of Toledo, Ohio, municipal water "do not drink" order that affected nearly 500,000 residents for 3 days. Given that microcystin degrading bacteria have been reported from HAB-affected waters around the world, we hypothesized that ...[more]

PMID: 32753778

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Project description:Microcystins are potent hepatotoxins that are frequently detected in fresh water lakes plagued by toxic cyanobacteria. Microbial biodegradation has been referred to as the most important avenue for removal of microcystin from aquatic environments. The biochemical pathway most commonly associated with the degradation of microcystin is encoded by the mlrABCD (mlr) cassette. The ecological significance of this pathway remains unclear as no studies have examined the expression of these genes in natural environments. Six metatranscriptomes were generated from microcystin-producing Microcystis blooms and analyzed to assess the activity of this pathway in environmental samples. Seventy-eight samples were collected from Lake Erie, United States/Canada and Lake Tai (Taihu), China, and screened for the presence of mlr gene transcripts. Read mapping to the mlr cassette indicated transcripts for these genes were absent, with only 77 of the collective 3.7 billion reads mapping to any part of the mlr cassette. Analysis of the assembled metatranscriptomes supported this, with only distantly related sequences identified as mlrABC-like. These observations were made despite the presence of microcystin and over 500,000 reads mapping to the mcy cassette for microcystin production. Glutathione S-transferases and alkaline proteases have been previously hypothesized to be alternative pathways for microcystin biodegradation, and expression of these genes was detected across space and time in both lakes. While the activity of these alternative pathways needs to be experimentally confirmed, they may be individually or collectively more important than mlr genes in the natural environment. Importantly, the lack of mlr expression could indicate microcystin biodegradation was not occurring in the analyzed samples. This study raises interesting questions about the ubiquity, specificity and locality of microcystin biodegradation, and highlights the need for the characterization of relevant mechanisms in natural communities to understand the fate of microcystin in the environment and risk to public health.

Project description:BackgroundCyanobacterial harmful algal blooms (CyanoHABs) originate from the excessive growth or bloom of cyanobacteria often referred to as blue-green algae. They have been on the rise globally in both marine and freshwaters in recently years with increasing frequency and severity owing to the rising temperature associated with climate change and increasing anthropogenic eutrophication from agricultural runoff and urbanization. Humans are at a great risk of exposure to toxins released from CyanoHABs through drinking water, food, and recreational activities, making CyanoHAB toxins a new class of contaminants of emerging concern.ObjectivesWe investigated the toxic effects and mechanisms of microcystin-LR (MC-LR), the most prevalent CyanoHAB toxin, on the ovary and associated reproductive functions.MethodsMouse models with either chronic daily oral or acute intraperitoneal exposure, an engineered three-dimensional ovarian follicle culture system, and human primary ovarian granulosa cells were tested with MC-LR of various dose levels. Single-follicle RNA sequencing, reverse transcription-quantitative polymerase chain reaction, enzyme-linked immunosorbent assay, western blotting, immunohistochemistry (IHC), and benchmark dose modeling were used to examine the effects of MC-LR on follicle maturation, hormone secretion, ovulation, and luteinization.ResultsMice exposed long term to low-dose MC-LR did not exhibit any differences in the kinetics of folliculogenesis, but they had significantly fewer corpora lutea compared with control mice. Superovulation models further showed that mice exposed to MC-LR during the follicle maturation window had significantly fewer ovulated oocytes. IHC results revealed ovarian distribution of MC-LR, and mice exposed to MC-LR had significantly lower expression of key follicle maturation mediators. Mechanistically, in both murine and human granulosa cells exposed to MC-LR, there was reduced protein phosphatase 1 (PP1) activity, disrupted PP1-mediated PI3K/AKT/FOXO1 signaling, and less expression of follicle maturation-related genes.DiscussionUsing both in vivo and in vitro murine and human model systems, we provide data suggesting that environmentally relevant exposure to the CyanoHAB toxin MC-LR interfered with gonadotropin-dependent follicle maturation and ovulation. We conclude that MC-LR may pose a nonnegligible risk to women's reproductive health by heightening the probability of irregular menstrual cycles and infertility related to ovulatory disorders. https://doi.org/10.1289/EHP12034.

Dataset Information

Isolation and Characterization of Lake Erie Bacteria that Degrade the Cyanobacterial Microcystin Toxin MC-LR.

Publications

Isolation and Characterization of Lake Erie Bacteria that Degrade the Cyanobacterial Microcystin Toxin MC-LR.

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