Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching

Abstract

Coral bleaching has been defined as a general phenomenon, whereby reef corals turn visibly pale because of the loss of their symbiotic dinof lagellates and͞or algal pigments during periods of exposure to elevated seawater temperatures. During the summer of 1997, seawater temperatures in the Florida Keys remained at or above 30°C for more than 6 weeks, and extensive coral bleaching was observed. Bleached colonies of the dominant Caribbean reefbuilding species, Montastrea faveolata and Montastrea franksi, were sampled over a depth gradient from 1 to 17 m during this period of elevated temperature and contained lower densities of symbiotic dinof lagellates in deeper corals than seen in previous ''nonbleaching'' years. Fluorescence analysis by pulse-amplitude modulation f luorometry revealed severe damage to photosystem II (PSII) in remaining symbionts within the corals, with greater damage indicated at deeper depths. Dinof lagellates with the greatest loss in PSII activity also showed a significant decline in the D1 reaction center protein of PSII, as measured by immunoblot analysis. Laboratory experiments on the temperature-sensitive species Montastrea annularis, as well as temperature-sensitive and temperature-tolerant cultured symbiotic dinof lagellates, confirmed the temperature-dependent loss of PSII activity and concomitant decrease in D1 reaction center protein seen in symbionts collected from corals naturally bleached on the reef. In addition, variation in PSII repair was detected, indicating that perturbation of PSII protein turnover rates during photoinhibition at elevated temperatures underlies the physiological collapse of symbionts in corals susceptible to heat-induced bleaching.Global episodes of coral bleaching, where reef-building corals lose their endosymbiotic dinoflagellates and͞or algal pigments during summertime elevation of seawater temperature, are recurring with increasing frequency and severity (1, 2). Previous studies have shown that symbiotic dinoflagellates maintained in culture and within the host are susceptible to thermal stress (3-5). Likewise, photosynthetically active radiation (PAR) and UV radiation may act in concert with elevated temperatures to elicit a bleaching response (6, 7), yet the underlying biochemical causes for these phenomena remain obscure. Numerous components of the photosynthetic pathway are known to be susceptible to damage by elevated temperature, especially at points within photosystem II (PSII). These include the oxygen-evolving complex (8, 9), the reaction center (10), as well as connectivity between the lightharvesting complex and the reaction center of PSII (11). In plants and green algae, thermal perturbation can predispose the photosynthetic apparatus to damage by PAR, thus inducing a state of photoinhibition (12). The primary target of photoinhibitory damage at the PSII reaction center is the D1 protein (13), which normally exhibits high rates of turnover involving light-dependent inactivation and degradation coupled with de novo synthesis and in...

Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae

“…The visible bleaching at 31 1C and 32 1C was preceded by drops in F v /F m , which declined by 53% and 80%, respectively after 7 days compared with CCA maintained at 27 1C. This reduction in F v /F m indicates potential chronic photoinactivation, caused by thermal and oxidative damage to (or loss of) the D1 reaction centre in PSII (Warner et al, 1999). In a recent study, the shallow CCA species Porolithon onkodes from the GBR also demonstrated partial bleaching following exposure to elevated SST (Anthony et al, 2008).…”

The physiological response of reef corals to diel fluctuations in seawater temperature

“…The effect of the treatment on Symbiodinium was assessed as maximum dark-adapted quantum yield of PSII (F V /F M [Genty et al, 1989]), which quantifies the efficiency of PSII (Jones et al, 1998;Warner et al, 1999). Decreases in F V /F M can signal chronic photoinhibition (damage to the photosynthetic apparatus), or reversible photoinhibition (Gorbunov et al, 2001).…”

Palau’s coral reefs show differential habitat recovery following the 1998-bleaching event

“…Coral bleaching is a consequence of high-irradiance and high water temperatures (Iglesias-Prieto et al 1992;Jones et al 1998;Warner et al 1999Warner et al , 2002Mumby et al 2001). Recently, it has been shown that the interrelatedness of temperature and light has reciprocal effects, whereby the increase in temperature under high light conditions will be perceived by the symbionts as an increase in light stress, and vice versa (Iglesias-Prieto et al 2004;Takahashi et al 2004;Nakamura et al 2005).…”