Inhibition of photosynthetic CO2 fixation in the coral Pocillopora damicornis and its relationship to thermal bleaching

Abstract

Two inhibitors of the Calvin-Benson cycle [glycolaldehyde (GA) and potassium cyanide (KCN)] were used in cultured Symbiodinium cells and in nubbins of the coral Pocillopora damicornis to test the hypothesis that inhibition of the Calvin-Benson cycle triggers coral bleaching. Inhibitor concentration range-finding trials aimed to determine the appropriate concentration to generate inhibition of the Calvin-Benson cycle, but avoid other metabolic impacts to the symbiont and the animal host. Both 3 mmol l(-1) GA and 20 μmol l(-1) KCN caused minimal inhibition of host respiration, but did induce photosynthetic impairment, measured by a loss of photosystem II function and oxygen production. GA did not affect the severity of bleaching, nor induce bleaching in the absence of thermal stress, suggesting inhibition of the Calvin-Benson cycle by GA does not initiate bleaching in P. damicornis. In contrast, KCN did activate a bleaching response through symbiont expulsion, which occurred in the presence and absence of thermal stress. While KCN is an inhibitor of the Calvin-Benson cycle, it also promotes reactive oxygen species formation, and it is likely that this was the principal agent in the coral bleaching process. These findings do not support the hypothesis that temperature-induced inhibition of the Calvin-Benson cycle alone induces coral bleaching.

Symbiodinium sp. cells produce light‐induced intra‐ and extracellular singlet oxygen, which mediates photodamage of the photosynthetic apparatus and has the potential to interact with the animal host in coral symbiosis

“…This hypothesis was tested using KCN and GA, which both block the Calvin–Benson cycle (Wishnick & Lane, ; Sicher, ). Incubation of Symbiodinium cells with 10 mM GA or 5 μM KCN has been shown to lead to a gradual loss of photosynthetic activity (Hill et al ., ), and here it was found that identical inhibitor treatments were accompanied by an enhanced level of 1 O 2 production (Fig. ).…”

“…However, trapping of intracellular 1 O 2 by externally added His ameliorates the inhibition of PSII electron transport, as well as the bleaching of Chls (Fig. ), which both occur under conditions of coral bleaching (Hill et al ., , ). These data demonstrate that 1 O 2 , which is formed inside Symbiodinium cells, is involved in the loss of PSII activity and also in the oxidative damage of the Chl pigments.…”

“…Measurements were performed in cultures with c . 10 μg Chl ml −1 (Takahashi et al ., ; Hill et al ., ).…”

Temperature Effects on the Growth Rates and Photosynthetic Activities of Symbiodinium Cells

“…Several hypotheses have been proposed to explain how elevated temperatures affect the photochemical pathway: excessive photon absorption by light harvesting antennae damages the PSII reaction center, particularly the D1 protein [17][18][19]; elevated temperatures may limit photosynthesis by destabilizing the thylakoid membranes [7]; the activity of Rubisco may be a primary site of damage by elevated temperature [20], though a recent study suggests that inhibition of the Calvin-Benson cycle alone does not induce coral bleaching [21]; damaged PSII reaction centers may be replaced by re-synthesized D1 protein, but this mechanism is inhibited when temperature is elevated [10]; elevated temperatures may also suppress the synthesis of light harvesting antennae protein at the translational step, thereby promoting losses of major light harvesting proteins [9]. Several of these postulates have been supported by recent studies indicating that the thermal stress susceptibility of Symbiodinium is determined by the repair capacity of the photosynthetic mechanism [10,22,23].…”

Sensitivity to oxidative stress is not a definite predictor of thermal sensitivity in symbiotic dinoflagellates

“…This results in reduced growth, respiration and photosynthetic rates, increased susceptibility to disease, and dramatically increased mortality of the symbiotic partners (Lesser 1996;Jones et al 1998;Hoegh-Guldberg et al 2007;Weis 2008). While the underlying cellular mechanisms responsible for bleaching have yet to be fully identified (Weis 2008;Weis et al 2008;Davy et al 2012), it has been suggested that higher temperatures primarily cause a negative impact on the light reactions of photosynthesis (Iglesias-Prieto et al 1992;Venn et al 2008), either through inhibition of PSII repair (Douglas 2003;Murata et al 2007;Takahashi and Murata 2008), damage to the thylakoid membranes of chloroplasts (Tchernov et al 2004;Venn et al 2008; but see Díaz-Almeyda et al 2011), or impairment of the CalvinBenson cycle, which leads to a build-up of excess energy in PSII (Jones et al 1998;Lilley et al 2010;Hill et al 2011Hill et al , 2014. However, a study by Tolleter et al (2013) found that coral bleaching can also occur with heat stress alone, in complete darkness.…”