Study of photosynthesis and alternative electron pathways in symbiotic cnidarians

The management of light energy during photosynthesis requires the concerted participation of multiple cellular processes, being the regulation of light absorption and the electron transfer in the photosynthetic machinery in the frontline. Due to the high diversity and divergence of microalgae groups, different molecular components can be found in their photosynthetic molecular machinery. Symbiodiniaceae, a family of dinoflagellates with a secondary-acquired peridinin chloroplast, contains a particular set of attributes. Members of this family perform mutualistic associations with a wide variety of animals, among which cnidarians are the most prominent. These photosynthetic cnidarians, such as the golden jellyfish Mastigias papua or the reef-building coral species Stylophora pistillata, obtain from their photosynthetic symbionts a variety of molecules to sustain their energetic demands, allowing them to participate as primary producers in marine ecosystems. The photosynthetic activity of these organisms have been documented, but details on the regulation of light absorption and photosynthetic electron transfer along their photosynthetic machinery is not well understood. In this work, the monitoring of the photosynthetic activity was addressed by spectroscopic methods, in order to provide information on the photosynthetic electron transfer activity of Symbidiniaceae in symbiosis with two cnidarians.
With the use of a chlorophyll a fluorescence imaging system we tracked the photosynthetic activity of the algal symbionts in the golden jellyfish M. papua. This jellyfish, together with its natural predator, the non-photosynthetic anemone Entacmaea medusivora, were collected from marine lakes in Palau, West Pacific. A peculiar phenomenon, observed during the field trip, brought a question on the fate of the algal symbiont, Cladocopium sp., when its host was digested by the anemone. The monitoring of the photosynthetic activity revealed that Cladocopium sp. was highly resistant to digestion, but it did not form an endosymbiotic association with the anemone. Moreover, the photosynthetic electron transfer activity remained unaffected during the digestion, and even after being expelled with non-digested fractions.
The coral S. pistillata was used to standardise a protocol for more specialised spectroscopic methods. Diverse technical problems have been an obstacle for the monitoring of the photochemical process in these organisms due to their calcareous skeleton. This issue was solved by fragmenting coral branches, a process that some corals experience naturally. The coral fragments of colonies grown in aquarium conditions were then used to provide information on the photosynthetic electron transfer process and the alternative electron transfer pathways in Symbiodiniaceae in symbiosis. The occurrence of these alternative pathways was thereafter shown in corals collected at mesophotic and shallow depths from a coral reef in the Gulf of Eilat, Israel. The photosynthetic activity of these coral colonies was compared, revealing differences in their sensitivity to light intensity and a differential use of the photosynthetic alternative electron pathways and photoprotection mechanisms. As part of the photoacclimation process of this coral species, the resistance of photosystem I to photoinhibition was observed.
Overall, in the symbiotic state, the Symbiodiniaceae species studied here showed a high resistance to harsh conditions, such as digestion of their jellyfish host by other animals, or by the mechanical stress when fragmenting their coral host. The photosynthetic activity of Symbiodiniaceae in symbiosis with S. pistillata, was found to present a series of photoacclimation strategies according to their environmental light conditions. Moreover, the photosynthetic activity of these algae include the use of photosynthetic alternative electron pathways. A feature that was found different from the information reported from algal cultures.