Abstract
Microcystins are cyanobacterial toxins that represent a serious threat to drinking water and recreational lakes worldwide. Here, we show that microcystin fulfils an important function within cells of its natural producer Microcystis. The microcystin deficient mutant ΔmcyB showed significant changes in the accumulation of proteins, including several enzymes of the Calvin cycle, phycobiliproteins and two NADPH-dependent reductases. We have discovered that microcystin binds to a number of these proteins in vivo and that the binding is strongly enhanced under high light and oxidative stress conditions. The nature of this binding was studied using extracts of a microcystin-deficient mutant in vitro. The data obtained provided clear evidence for a covalent interaction of the toxin with cysteine residues of proteins. A detailed investigation of one of the binding partners, the large subunit of RubisCO showed a lower susceptibility to proteases in the presence of microcystin in the wild type. Finally, the mutant defective in microcystin production exhibited a clearly increased sensitivity under high light conditions and after hydrogen peroxide treatment. Taken together, our data suggest a protein-modulating role for microcystin within the producing cell, which represents a new addition to the catalogue of functions that have been discussed for microbial secondary metabolites.
Highlights
Microcystis is a unicellular colonial cyanobacterium frequently developing blooms in freshwater habitats [1]
Loss of microcystin leads to an altered accumulation of specific proteins in M. aeruginosa PCC 7806
In an earlier study we showed a fast rise in the accumulation of mcy mRNA encoding microcystin biosynthesis enzymes in Microcystis cells exposed to light intensities higher than about 50 mmol photons m22 s21 [13]
Summary
Microcystis is a unicellular colonial cyanobacterium frequently developing blooms in freshwater habitats [1]. Buoyant colonies may form thick scums at the surface of lakes where they are exposed to high light. Even under these high irradiances, Microcystis shows high photosynthesis rates, thereby maintaining numerical dominance in eutrophic waters when physico-chemical conditions favour bloom formation [2]. Microcystin intoxications can affect humans and livestock as well as various cyanobacterial grazers such as Daphnia (see [4] and references therein). Feeding experiments revealed that Microcystis strains can inhibit grazing activity of Daphnia regardless of the occurrence of microcystins [5,6]. A phylogenetic analysis of the microcystin biosynthesis genes (mcy) among diverse cyanobacterial genera revealed that they co-evolved with house-keeping genes and clearly preceded the appearance of the metazoans, i.e. well ahead of the potential grazers [7]
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