Abstract
The ubiquitous freshwater cyanobacterium Microcystis is remarkably successful, showing a high tolerance against fluctuations in environmental conditions. It frequently forms dense blooms which can accumulate significant amounts of the hepatotoxin microcystin, which plays an extracellular role as an infochemical but also acts intracellularly by interacting with proteins of the carbon metabolism, notably with the CO2 fixing enzyme RubisCO. Here we demonstrate a direct link between external microcystin and its intracellular targets. Monitoring liquid cultures of Microcystis in a diel experiment revealed fluctuations in the extracellular microcystin content that correlate with an increase in the binding of microcystin to intracellular proteins. Concomitantly, reversible relocation of RubisCO from the cytoplasm to the cell’s periphery was observed. These variations in RubisCO localization were especially pronounced with cultures grown at higher cell densities. We replicated these effects by adding microcystin externally to cultures grown under continuous light. Thus, we propose that microcystin may be part of a fast response to conditions of high light and low carbon that contribute to the metabolic flexibility and the success of Microcystis in the field.
Highlights
Cyanobacterial strains of the genus Microcystis are infamous for the formation of freshwater blooms, which pose a threat to humans and animals due to the production of the potent hepatotoxin microcystin (MC) [1]
Given that previous studies reported a major impact of the cellular density of Microcystis cultures on both the secretion of MC and the binding of MC to proteins, we cultivated liquid cultures of Microcystis at two different cell densities with a 16 h:8 h light:dark photoperiod
Microcystin plays an important intracellular role that seems to be rooted in the central carbon metabolism
Summary
Cyanobacterial strains of the genus Microcystis are infamous for the formation of freshwater blooms, which pose a threat to humans and animals due to the production of the potent hepatotoxin microcystin (MC) [1]. Climate change and increasing eutrophication in lakes further promote the mass development of these cyanobacteria that leads to an ecological collapse in affected freshwater habitats connected with a considerable economic loss [2,3]. The cyclic heptapeptide MC is produced by a giant non-ribosomal peptide synthetase (NRPS) assembly line linked with high metabolic costs for the producing cells [4]. While the ability to produce the cyanotoxin and other non-ribosomal peptides was lost in many cyanobacterial phyla it was retained in phylogenetically distant bloom-forming species suggesting a close connection to the bloom-forming lifestyle [5].
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