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The Cyanotoxin BMAA Induces Heterocyst Specific Gene Expression in Anabaena Sp. PCC 7120 Under Repressive Conditions

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The Cyanotoxin BMAA Induces Heterocyst Specific Gene Expression in Anabaena Sp. PCC 7120 Under Repressive Conditions

Alexandra A Popova et al. Toxins (Basel).

Abstract

Cyanobacteria synthesize neurotoxic β-N-methylamino-l-alanine (BMAA). The roles of this non-protein amino acid in cyanobacterial cells are insufficiently studied. During diazotrophic growth, filamentous cyanobacteria form single differentiated cells, called heterocysts, which are separated by approximately 12⁻15 vegetative cells. When combined nitrogen is available, heterocyst formation is blocked and cyanobacterial filaments contain only vegetative cells. In the present study, we discovered that exogenous BMAA induces the process of heterocyst formation in filamentous cyanobacteria under nitrogen-replete conditions that normally repress cell differentiation. BMAA treated cyanobacteria form heterocyst-like dark non-fluorescent non-functional cells. It was found that glutamate eliminates the BMAA mediated derepression. Quantitative polymerase chain reaction (qPCR) permitted to detect the BMAA impact on the transcriptional activity of several genes that are implicated in nitrogen assimilation and heterocyst formation in Anabaena sp. PCC 7120. We demonstrated that the expression of several essential genes increases in the BMAA presence under repressive conditions.

Keywords: BMAA; cyanobacteria; cyanotoxin; gene expression; heterocyst differentiation.

Conflict of interest statement

The authors declare that they have no conflicts of interest.

Figures

Figure 1
Figure 1
Filaments of Anabaena 7120 on different nitrogen sources after 72 h of cultivation are shown. (A) Anabaena 7120 grown on BG110; (B) Anabaena 7120 grown on BG11N with 17 mM sodium nitrate; (C) Anabaena 7120 grown on BG11N with 17 mM sodium nitrate and 20 µM BMAA; (D) Anabaena 7120 grown on BG11N with 5 mM ammonium chloride; (E) Anabaena 7120 grown on BG11N with 5 mM ammonium chloride and 100 µM BMAA; (F) cyanobacteria after 72 h of incubation with 20 µM BMAA and 250 µM glutamate on nitrate-containing medium. On the left panels, cyanobacterial filaments are shown as a combination of light field and fluorescent images. The right panels show autofluorescence of chlorophyll. Heterocyst-like cells do not show fluorescence (arrows).
Figure 2
Figure 2
Anabaena 7120 filaments with multiple heterocyst-like cells after 72 h of cultivation on nitrate with BMAA (20 µM) are presented. On the left panel, cyanobacterial filament is shown as a combination of light field and fluorescent images. The right panel shows autofluorescence of chlorophyll. Heterocyst-like cells are nonfluorescent (arrows).
Figure 3
Figure 3
Dependence of heterocyst-like cells frequency on BMAA concentrations is shown. Anabaena 7120 cells were exposed with BMAA for 72 h in the medium containing ammonium (5 mM) (as nitrogen source).
Figure 4
Figure 4
Filaments of Nostoc sp. strain 8963 after 72 h of cultivation on nitrate-medium are presented. (A) Nostoc sp. strain 8963 with 100 µM BMAA treatment; (B) Nostoc sp. strain 8963 without BMAA treatment. On the left panels, cyanobacterial filaments are shown as a combination of light field and fluorescent images. The right panels show autofluorescence of chlorophyll. Heterocyst-like cell does not show fluorescence (arrows).

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