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Microcystins and Microcystis aeruginosa PCC7806 extracts modulate steroidogenesis differentially in the human H295R adrenal model.

ABSTRACT: The aim of this study was to investigate the potential interference of cyanobacterial metabolites, in particular microcystins (MCs), with steroid hormone biosynthesis. Steroid hormones control many fundamental processes in an organism, thus alteration of their tissue concentrations may affect normal homeostasis. We used liquid chromatography-tandem mass spectrometry (LC-MS/MS) to investigate the modulation of 14 hormones involved in the adrenal steroid biosynthesis pathway using forskolin-treated H295R cells, following exposure with either microcystin-LR (MC-LR) alone, a mixture made up of MC-LR together with eight other MCs and nodularin-R (NOD-R), or extracts from the MC-LR-producing Microcystis aeruginosa PCC7806 strain or its MC-deficient mutant PCC7806mcyB-. Production of 17-hydroxypregnenolone and dehydroepiandrosterone (DHEA) was increased in the presence of MC-LR in a dose-dependent manner, indicating an inhibitory effect on 3?-hydroxysteroid dehydrogenase (3?-HSD). This effect was not observed following exposure with a MCs/NOD-R mixture, and thus the effect of MC-LR on 3?-HSD appears to be stronger than for other congeners. Exposure to extracts from both M. aeruginosa PCC7806 and M. aeruginosa PCC7806mcyB- had an opposite effect on 3?-HSD, i.e. concentrations of pregnenolone, 17-hydroxypregnenolone and DHEA were significantly decreased, showing that there are other cyanobacterial metabolites that outcompete the effect of MC-LR, and possibly result instead in net-induction. Another finding was a possible concentration-dependent inhibition of CYP21A2 or CYP11?1, which catalyse oxidation reactions leading to cortisol and cortisone, by MC-LR and the MCs/NOD-R mixture. However, both M. aeruginosa PCC7806 and M. aeruginosa PCC7806mcyB- extracts had an opposite effect resulting in a substantial increase in cortisol levels. Our results suggest that MCs can modulate steroidogenesis, but the net effect of the M. aeruginosa metabolome on steroidogenesis is different from that of pure MC-LR and independent of MC production.

SUBMITTER: Mallia V

PROVIDER: S-EPMC7737990 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Microcystins and Microcystis aeruginosa PCC7806 extracts modulate steroidogenesis differentially in the human H295R adrenal model.

Mallia Vittoria V Verhaegen Steven S Styrishave Bjarne B Eriksen Gunnar Sundstøl GS Johannsen Malene Louise ML Ropstad Erik E Uhlig Silvio S

PloS one 20201215 12

The aim of this study was to investigate the potential interference of cyanobacterial metabolites, in particular microcystins (MCs), with steroid hormone biosynthesis. Steroid hormones control many fundamental processes in an organism, thus alteration of their tissue concentrations may affect normal homeostasis. We used liquid chromatography-tandem mass spectrometry (LC-MS/MS) to investigate the modulation of 14 hormones involved in the adrenal steroid biosynthesis pathway using forskolin-treate ...[more]

PMID: 33320886

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Project description:Microcystis aeruginosa is a cosmopolitan cyanobacteria that continues to jeopardize freshwater ecosystem services by releasing the hepatotoxin microcystin, which can, in some cases, cause death to aquatic fauna and even humans. Currently, our abilities to understand the mechanisms of microcystin toxicology are limited by the lack of a method for producing high concentrations, which are central to large-scale and long-term research in natural systems. Here we present an efficient and affordable laboratory method to produce high concentrations of microcystins by a toxigenic strain of M. aeruginosa. Through batch culture studies, we yielded microcystins at concentrations that are environmentally relevant to freshwaters around the world (1-300 μg L-1), maintained these concentrations without resupplying fresh medium (further reducing costs), and utilized rate equations to model the relationship between the environmental conditions in the cultures and changes occurring within the M. aeruginosa cells. Our assessment suggests that steady production of microcystins depends on the availability of carbon throughout the experiment. Hence, we recommend the use of tissue culture treated flasks with a vented cap to ensure the production of microcystins is uninterrupted. This method demonstrates that microcystins can be produced in the laboratory at concentrations relevant to freshwater ecosystems. •The method demonstrates M. aeruginosa CPCC 300 is a reliable strain of freshwater cyanobacteria that can yield microcystins at environmentally relevant concentrations.•Validation showed M. aeruginosa CPCC 300 is resilient in carbon-limited situations and may respond to stress by shifting the ratio of microcystin congeners.•Cell culture flasks with vented caps -filled no more than 50 % of the flask volume to allow for sufficient air exchange- are an excellent and cost-effective approach to maintaining cell growth and producing microcystins at a range between 300 to 1200 μg L-1.

Project description:Introduction: Toxic microcystins (MCs) produced by cyanoprokaryotes -particularly by the cosmopolitan cyanobacterium Microcystis aeruginosa- pose adverse effects on aquatic organisms and their ecosystem and may also cause serious impacts on human health. These harmful monocyclic heptapeptides are the most prevalent cyanotoxins reported in freshwaters and must be eliminated for avoiding MCs release in receiving water bodies. Hence, this work aimed to test the efficacy of Moringa oleifera seeds water-based extract (MO) as a natural coagulant for removing cyanobacteria (especially M. aeruginosa), microalgae, and its associated MCs from pre-treated municipal wastewaters. Methodology: Four different MO coagulant doses (25, 50, 75 and 100 mg L-1) were investigated for cyanobacteria and microalgae removal by conventional coagulation assays and morphology-based taxonomy studies. Additionally, water turbidity and chlorophyll a (Chl a) content were also determined. Further, the presence and concentration of MCs soluble in water, remaining in the particulate fraction, and flocculated within the residual sludge were assessed using high-performance liquid chromatography coupled with diode array detection (HPLC-DAD). Results: The treatment with MO at 100 mg L-1 substantially reduced the number of cyanobacterial and microalgal species in the treated samples (average removal rate of 93.8% and 86.9%, respectively). These results agreed with a ∼44% concomitant reduction in Chl a and ∼97% reduction in water turbidity (a surrogate marker for suspended solids content). Notably, MCs concentrations in the treated water were significantly lowered to 0.6 ± 0.1 µg L-1 after addition of 100 mg L-1 MO. This value is below the WHO recommended limits for MCs presence in drinking water (<1.0 µg L-1). Discussion: The present study provides promising insights into the applicability of MO as a cost-effective, reliable, and sustainable natural coagulant, particularly for using in developing countries, to eliminate harmful cyanobacteria and cyanotoxins in municipal water treatment facilities.

Dataset Information

Microcystins and Microcystis aeruginosa PCC7806 extracts modulate steroidogenesis differentially in the human H295R adrenal model.

Publications

Microcystins and Microcystis aeruginosa PCC7806 extracts modulate steroidogenesis differentially in the human H295R adrenal model.

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