Different ecophysiological and structural strategies of toxic and non-toxic Microcystis aeruginosa (cyanobacteria) strains assessed under culture conditions

Abstract

Microcystis aeruginosa causes severe problems in freshwater environments worldwide due to its capacity to form blooms and produce toxins. Natural populations contain a mixture of strains that vary in morphology, genotype and microcystin production. Beyond its toxic effect in animals, the possible role of microcystin in the metabolism of the producing cell is also a topic of interest. Recent studies pointed to a protective role against cellular oxidative stress. Since natural populations include microcystin producing and non-producing strains, the latter must rely on other ecophysiological traits to thrive. Here, we compared a toxic and a non-toxic strain of M. aeruginosa displaying different morphotypes and growth behaviors, aiming to explore the role of microcystin in an integrated way to the primary metabolism. The toxic strain formed large floating colonies (150–1850 μm) with densely aggregated cells, numerous gas vesicles and lipid inclusions and a typical irregular thylakoid arrangement. The non-toxic strain remained submerged, formed small colonies (< 100 μm) with a dense mucilage covering few sparse cells with rare gas vesicles and various types of thylakoids. It showed a higher abundance of carboxysomes, cyanophycin and polyphosphate granules and also greater amounts of pigments than the toxic strain. The antioxidant potential was higher for the toxic strain and it presented a higher expression of proteins related to photosynthesis, protein folding and cellular redox homeostasis. These traits of the toxic strain were compatible with growth under higher irradiance and microcystin can be a key factor to this adaptation. Growing submerged, the non-toxic strain showed preference for a lower light intensity and invested in intracellular reserves. This study illustrates different adaptive strategies of M. aeruginosa morphotypes that can be valuable in nature, enabling this species to widely exploit freshwater ecosystems.