Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium

Abstract

Coral bleaching, caused by heat stress, is accompanied by the light-induced loss of photosynthetic pigments in in situ symbiotic dinoflagellate algae (Symbiodinium spp.). However, the molecular mechanisms responsible for pigment loss are poorly understood. Here, we show that moderate heat stress causes photobleaching through inhibition of the de novo synthesis of intrinsic lightharvesting antennae [chlorophyll a-chlorophyll c 2-peridininprotein complexes (acpPC)] in cultured Symbiodinium algae and that two Clade A Symbiodinium species showing different thermal sensitivities of photobleaching also show differential sensitivity of this key protein synthesis process. Photoinhibition of photosystem II (PSII) and subsequent photobleaching were observed at temperatures of >31°C in cultured Symbiodinium CS-73 cells grown at 25-34°C, but not in cultures of the more thermally tolerant control Symbiodinium species OTcH-1. We found that bleaching in CS-73 is associated with loss of acpPC, which is a major antennae protein in Symbiodinium. In addition, the thermally induced loss of this protein is light-dependent, but does not coincide directly with PSII photoinhibition and is not caused by stimulated degradation of acpPC. In cells treated at 34°C over 24 h, the steady-state acpPC mRNA pool was modestly reduced, by Ϸ30%, whereas the corresponding synthesis rate of acpPC was diminished by >80%. Our results suggest that photobleaching in Symbiodinium is consequentially linked to the relative susceptibility of PSII to photoinhibition during thermal stress and occurs, at least partially, because of the loss of acpPC via undefined mechanism(s) that hamper the de novo synthesis of acpPC primarily at the translational processing step.bleaching ͉ photoinhibition ͉ zooxanthellae ͉ coral ͉ symbiosis

Increased rate of D1 repair in coral symbionts during bleaching is insufficient to counter accelerated photo‐inactivation

“…Nishiyama et al (2006) found that stress from reactive oxygen species (ROS) manifests as inhibition to PSII repair, whereas optical changes or changes in PSII organisation would manifest as altered susceptibility to primary photo-inactivation. Our data thus show that increased susceptibility to photo-inactivation, rather than an inhibition of PSII repair (Nishiyama et al 2006), is the principal trigger for net photo-inhibition of PSII activity under these bleaching conditions in hospite, in contrast to the recent findings of Takahashi et al (2009) on cultured, Clade A Symbiodinium. Despite their elevated PSII repair rates during bleaching, the symbionts were unable to counteract the increased rate of photo-inactivation provoked by the combination of increased temperature and an An alternate bleaching hypothesis has attributed the initial weakness to damage to the dark reaction of the zooxanthellae (Jones et al 1998).…”

“…This supports previous studies that show coral bleaching only occurs during a combination of elevated light and temperature (Brown 1997). The application of our bleaching treatment (a concomitant increase in irradiance and temperature), does not allow for distinction between independent effects of light and temperature, but thermal stress is well-known to increase the susceptibility of coral symbionts to light-induced PSII photo-inactivation (Bhagooli and Hidaka 2004;Takahashi et al 2008;Hill et al 2009). …”

Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species

“…These results demonstrated that CS-73 is much more sensitive to photoinhibition associated with thermal stress than OTcH-1, as shown in ref. 26.…”

“…However, it should be noted that the sensitivities of photoinhibition and coral bleaching are not determined only by the properties of the Symbiodinium species, because host factors, such as the production of host pigments (34,35) and the colony morphology of corals (36), also have the potential to influence these sensitivities. Recent studies have demonstrated that thermally induced photoinhibition is strongly associated with coral bleaching caused by photobleaching of photosynthetic pigments in individual Symbiodinium in corals (21,26). Whether photoinhibition on its own or in concert with broader physiological events in symbiont and host causes expulsion of Symbiodinium from corals remains unqualified (37), although there are many reports showing that thermally induced loss of Symbiodinium is accompanied by photoinhibition (4,7,8,38).…”

“…Total amount of Chl was extracted and measured as shown in ref. 26. Temperature treatments were performed in 1-mL glass vials incubated in an aluminum heat gradient block.…”