Analysis of Symbiodinium microadriaticum mutant strains with impaired PSII activity

The eukaryotic tree bears numerous taxa that have lost the photosynthetic capacities of their ancestors. In the presence of an alternative source of energy, the need for photosynthesis declines and the electron transport machinery can be partially to completely dropped over generations. Despite its large distribution across Eukaryotes, this shift to heterotrophism is still poorly understood, particularly its onset. To explore this topic, we examined Symbiodinium microadriaticum, which belongs to dinoflagellates, a phylum where the loss of photosynthesis has occurred particularly frequently.
Glucose-requiring mutant strains were isolated from S. microadriaticum cultivated in conditions supplemented with glucose and amino acids. These strains were identified as lacking chloroplastic genes encoding proteins essential for photosynthesis. We focused on the physiology of two specific strains, deficient either for PSBI or PSBE proteins, which are anticipated to play a role in the assembly or repair of photosystem II (PSII).
Our findings reveal that the psbI strain exhibits limited growth in minimal medium, while its growth was rescued in supplemented medium. The absence of PSBI results in a decreased activity of PSII, as indicated by reduced maximum photosynthetic yield and relative electron transport rate through PSII, whereas the activity of PSI remains similar to that of the wild-type strain. Conversely, the psbE strain displays a more pronounced phenotype, relying entirely on glucose and amino acid supplementation for growth and carrying a completely inactive PSII. However, sustained activity of PSI was also observed in this strain. The imbalance between PSII and PSI was corroborated in both strains by analysis of the electrochromic shift. This PSII-independent PSI activity suggests that these strains leverage a circular electron flow around PSI, leading to the establishment of a proton gradient across the thylakoid membrane.
In conclusion, the analysis of these mutant strains suggests that survival of Symbiodinium microadriaticum is achievable with a weakened or inactive PSII in the presence of an external energy source and with a fully functional PSI. Beside their evolutionary significance, these strains represent a valuable opportunity to conduct comprehensive studies on the photosynthetic complexes within this model organism.