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Abstract
Toxin synthesis in bloom-forming cyanobacterial communities is a dynamic process that responds to changes in the environment, such as light, nutrient availability and oxidative stress. Our limited understanding of the factors that drive bloom formation, and the increased incidence of cyanobacterial blooms worldwide present a significant challenge to the water industry. The production of the hepatotoxic non-ribosomal peptide microcystin has been proposed to be advantageous to toxic cells and appears to be regulated by nitrogen- and iron-stress responsive proteins at the transcriptional level. In this study, protein expression in the unicellular microcystin-producing Microcystis aeruginosa species was investigated in nutrient-replete and nutrient-stress conditions.
The proteome of M. aeruginosa was highly strain-specific, with protein expression changes accumulating during prolonged growth in laboratory culture. Microcystin synthesis was found to be a dynamic trait in toxigenic, but inactive M. aeruginosa strains, and the reversal of one such previously non-toxic strain to toxicity was reported. Transcription of the mcyA gene involved in microcystin synthesis was also identified in both toxic and non-toxic strains and suggests that regulation of toxin synthesis occurs at the post-transcriptional level.
In nutrient-replete conditions proteins differentially displayed between toxic and nontoxic M. aeruginosa were targets of the global nitrogen control transcriptional regulator NtcA and were involved in carbon fixation, nitrogen metabolism and redox balance. The iron starvation response in M. aeruginosa appeared to result from differential transcription of ferric uptake regulators (Fur), which affected processes involved in iron uptake and modification of the photosynthetic machinery. Iron, but not nitrogen stress, induced microcystin synthesis and prevented chlorosis in the model toxic PCC 7806 strain. In nitrogen-limited growth, the protein expression profiles of M. aeruginosa supported an active involvement of NtcA in the stress response of non-toxic strains. These results suggest that NtcA metabolic control is affected by microcystin synthesis and the nutrient status of the cells, leading to differences in the C:N ratio in toxic and non-toxic cells. This could underpin the differential response of strains of M. aeruginosa to changes in the environment. Further global expression studies of hepatotoxic cyanobacteria are required before reliable bloom control protocols can be established.