Hydrogen peroxide and nitric oxide trigger redox-related cyst formation in cultures of the dinoflagellate Lingulodinium polyedrum

- Five hundred micromolar H2O2 forced Lingulodinium polyedrum to rapidly encyst (<30 min), whereas slower encystment occurs upon lower H2O2 doses.
- Orchestrated antioxidant responses from the carotenoid peridinin and ascorbate peroxidase diminished lipid oxidation during cyst formation.
- N-assimilation and photosynthesis are dispensable processes during encystment.
- Although apparently less efficient than H2O2, similar antioxidant responses were observed in NO-treated cultures.
- H2O2 and NO were confirmed as key redox signals since oxidative stress dictates the progression of cyst formation in Lingulodinium polyedrum.

The dinoflagellate Lingulodinium polyedrum is a toxin producer that shows the ability of turning to resting cysts as a survival strategy when exposed to environmental unfavorable conditions, such as nitrogen and phosphorus depletion, abrupt changes in temperature or light, and chemical or mechanical stress. Algal adaptation to all these conditions involves hydrogen peroxide (H2O2) and nitric oxide (NO) as key redox signals for housekeeping cellular processes. Thus, we aim here to shed light on the role of H2O2 and NO (from aqueous decomposition of sodium nitroprusside, SNP) as prooxidant agents and putative redox signals for encystment of the dinoflagellate L. polyedrum. Harsh oxidative stress imposed by 500 μM H2O2 treatment forced L. polyedrum cells to rapidly encyst, in less than 30 min, whereas slower cyst formation was observed upon lower H2O2 doses. L. polyedrum encystment was marked by a significant increase in the antioxidant carotenoid peridinin, although other photosynthetic pigments (chlorophyll a and β-carotene) and light-harvesting complexes (peridinin complex protein, PCP) were all diminished in cyst forms. Although SOD activity (a frontline antioxidant enzyme) was severely inhibited by increasing doses of H2O2, a theoretical compensatory effect was provided by the dose-dependent increase of ascorbate peroxidase activity (APX), which resulted in significant lower levels of lipid peroxidation during cyst formation. Although SNP data cannot be fully compared to those found with H2O2 treatments, changes in APX activity and in biomarkers of lipid and protein oxidation matched the dose-responses found in H2O2 experiments, revealing similar biochemical and morphological responses against increasing oxidative conditions during cyst formation. Our data significantly contribute to a better understanding of the relationship between encystment, photosynthesis, and antioxidant responses triggered by H2O2 and NO in L. polyedrum, a harmful diarrhetic shellfish poisoning toxin (DSPs) producer.