“Super-quenching” state protects Symbiodinium from thermal stress — Implications for coral bleaching

• Published in: Biochimica et biophysica acta Vol. 1857; no. 6; pp. 840 - 847
• Main Authors: Slavov, Chavdar, Schrameyer, Verena, Reus, Michael, Ralph, Peter J., Hill, Ross, Büchel, Claudia, Larkum, Anthony W.D., Holzwarth, Alfred R.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.06.2016
• Subjects: Animals; Anthozoa - parasitology; Chlorophyll - metabolism; Coral bleaching; Dinoflagellida - metabolism; Dinoflagellida - physiology; Dinoflagellida - ultrastructure; Electron Transport - radiation effects; Global climate change; Kinetics; Light; Luminescent Measurements - methods; Microscopy, Electron, Transmission; Models, Biological; Non-photochemical quenching; Oxidation-Reduction - radiation effects; Photosynthesis; Photosynthesis - radiation effects; Photosystem I Protein Complex - metabolism; Photosystem II Protein Complex - metabolism; Stress, Physiological - physiology; Symbiodinium; Symbiosis; Symbiosis - physiology; Temperature; Thylakoids - metabolism; Thylakoids - radiation effects; Time Factors; Symbiosis; Chl; PSII; Non-photochemical quenching; PSI; FHL; NPQ; Symbiodinium; LHCs; RC; Coral bleaching; FHT; PSU; SI; DAS; FWHM; SAES; Global climate change; FB; Photosynthesis; FC; TEM; RP; PSA
• ISSN: 0005-2728; 0006-3002; 1879-2650
• DOI: 10.1016/j.bbabio.2016.02.002

The global rise in sea surface temperatures causes regular exposure of corals to high temperature and high light stress, leading to worldwide disastrous coral bleaching events (loss of symbiotic dinoflagellates (Symbiodinium) from reef-building corals). Our picosecond chlorophyll fluorescence experiments on cultured Symbiodinium clade C cells exposed to coral bleaching conditions uncovered the transformations of the alga's photosynthetic apparatus (PSA) that activate an extremely efficient non-photochemical “super-quenching” mechanism. The mechanism is associated with a transition from an initially heterogeneous photosystem II (PSII) pool to a homogeneous “spillover” pool, where nearly all excitation energy is transferred to photosystem I (PSI). There, the inherently higher stability of PSI and high quenching efficiency of P700+ allow dumping of PSII excess excitation energy into heat, resulting in almost complete cessation of photosynthetic electron transport (PET). This potentially reversible “super-quenching” mechanism protects the PSA against destruction at the cost of a loss of photosynthetic activity. We suggest that the inhibition of PET and the consequent inhibition of organic carbon production (e.g. sugars) in the symbiotic Symbiodinium provide a trigger for the symbiont expulsion, i.e. bleaching. [Display omitted] •Stress factors causing coral bleaching were investigated in cultured Symbiodinium.•Ultrafast chlorophyll fluorescence was used to detect the photosynthetic responses.•Excitation energy migrates to photosystem I where it is quenched — super-quenching.•The super-quenching short-circuits PSII, which interrupts linear electron transport.•Cessation of photosynthetic activity could trigger Symbiodinium expulsion in situ.