Mixotrophic flagellate Ochromonas gloeopara promotes heterocyst production in cyanobacteria with altered filament length

Abstract

Heterocystous cyanobacteria can adapt to environmental fluctuations typically via the production of heterocyst, a specialized cell functioning dinitrogen-fixing. Responses of heterocyst production to abiotic stressors like nutrient availability have been widely studied. In natural environments cyanobacteria also face great pressures from a variety of organisms including mixotrophic protists. However, little is known about the impacts of mixotrophic protists on the filamentous cyanobacteria characterized by heterocyst production. Here, we explored the grazing of the flagellate Ochromonas gloeopara on two heterocystous cyanobacteria Dolichospermum flos-aquae and Anabaena sp., together with the cyanobacterial responses in terms of population growth, heterocyst production, filament length and photosynthesis. Results showed that O. gloeopara preyed on short filaments of both cyanobacteria, reducing the population growth rate of D. flos-aquae but not the Anabaena sp. The average filament length of the two species was generally increased by O. gloeopara grazing at the initial cultivation, whereas reversed phenomenon was observed in Anabaena sp. at late cultivation. O. gloeopara presence promoted the heterocyst production in both the cyanobacteria, with heterocyst abundance showing a rapid increase followed by decrease dynamic with cultivation. Heterocyst placement pattern was also changed with the number of vegetative cells between heterocysts increased in Anabaena sp. At the peak phase of heterocyst production, the maximum quantum efficiency of photosynthesis in D. flos-aquae enhanced as response to O. gloeopara presence. These findings reveal a phenotypic adaptation of heterocystous cyanobacteria to pressures from mixotrophic protists, providing a new perspective for understanding the role of biotic interactions in cyanobacterial blooms.