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Photosynthetic organisms must maintain a balance between the interception of light energy, the supply of this excitation energy to the photosynthetic reaction centres, the production of NADPH and ATP within the thylakoid membranes, and the utilization of NADPH and ATP for CO2 fixation and for biosynthesis. Changes in photosynthetic photon flux density (PFD) on timescales of seconds to days affect this balance, and as a consequence plants and algae must employ a range of mechanisms to adjust their physiologies to maintain this balance (Raven & Geider, 2003; Falkowski & Raven, 2007).
Photoacclimation is the term used to designate the process of adjustment of the phenotype of plants, algae and cyanobacteria to changes in the light environment. It operates on timescales of hours to days, which are intermediate between rapid changes involved in the regulation of enzyme activities and long timescales associated with changes in adaptation of the genotype (Raven & Geider, 2003). Photoacclimation involves changes in ultrastructure, morphology, biochemical and elemental composition, pigment content (Falkowski & La Roche, 1991), and the composition of the proteome (Pandhal et al., 2007; McKew et al., 2013).
The contrasting demands of aquatic and terrestrial environments, and the contrasting lifestyles of multicellular vascular plants and unicellular microalgae have led to differences in evolutionary adaptations and strategies of physiological acclimation (Geider et al., 2001). For example, many vascular plant leaves photoacclimate to high light by increasing the abundance of Calvin cycle enzymes per unit area whilst maintaining light absorption (Seemann et al., 1987; Givnish, 1988), whereas microalgae reduce light harvesting without increasing Calvin cycle enzymes (Sukenik et al., 1987; McKew et al., 2013). These differences in acclimatory strategy are likely to be a consequence of the fact that vascular plant leaves are optically thick and absorb > 90% of incident solar radiation (Knapp & Carter, 1998), whereas microalgae are typically optically thin and absorb < 50% of the light that falls on their surfaces (Morel & Bricaud, 1981). Additionally, vascular plants can often be characterized into sun and shade ecotypes (Givnish, 1988), whereas most microalgae and cyanobacteria are evolutionarily adapted to low light (Richardson et al., 1983), although a few notable exceptions of high and low light ecotypes have been identified (Moore & Chisholm, 1999). Within the microalgae and cyanobacteria, the rate of photosynthesis is typically saturated at c. 50–400 μmol photons m−2 s−1 (Richardson et al., 1983), which is significantly less than full noon sunlight. In most ocean environments photosynthesis shows a subsurface maximum at a depth corresponding to c. 10–30% of surface PFD (Behrenfeld & Falkowski, 1997), whereas in many vascular plants photosynthesis of ‘sun’ leaves does not saturate even in full sunlight (Bjorkman, 1981).
Photoacclimation on timescales of hours to days affects important physiological processes including the light dependence of photosynthesis and the susceptibility of photosystem II (PSII) reaction centres (RCII) to photoinactivation (Richardson et al., 1983; Falkowski & La Roche, 1991; Raven & Geider, 2003). During acclimation to incident light, microalgae modify components associated with PSII and photosystem I (PSI), (Falkowski & Raven, 2007). These adjustments appear to be driven, in part, through redox and reactive oxygen species (ROS) signalling that arise from an imbalance between the rate of light absorption and the rate of energy consumption in photosynthesis and biosynthesis (Escoubas et al., 1995; Pfannschmidt et al., 2009), although blue-light receptors have also been implicated in the photoacclimation of diatoms (Schellenberger Costa et al., 2013).
Knowledge of the cost–benefit trade-offs involved in photoacclimation is essential for developing a mechanistic understanding of how photosynthetic organisms acclimate to the light environment in order to improve fitness (Geider et al., 2009). These costs and benefits can be evaluated within the context of three design considerations for structure–function relationships in chloroplasts (Raven, 1980). These are the energetic efficiency of photosynthesis (work output divided by energy input), the catalytic efficiency of photosynthesis (work output per unit catalytic and structural material contained in the chloroplast) and the provision of mechanisms to ensure safe operation of the photosynthetic apparatus. Such an analysis is facilitated by the fact that all oxygenic photoautotrophs possess a highly conserved light-driven energy transduction pathway linking O2 evolution by PSII to the production of triose phosphates in the Calvin cycle (Blankenship, 2002). By contrast, considerable phylogenetic diversity is evident upstream of PSII in the light-harvesting pigments and proteins amongst the cyanobacteria and the green and red algal lineages (Blankenship, 2002), as well as in the downstream metabolism of the products of CO2 fixation (Wilhlem et al., 2006). This includes differences in organic C storage products, with carbohydrates or neutral lipids the major storage products depending on species and growth condition (Lacour et al., 2012).
In this paper, we examine photoacclimation of the marine haptophyte Emiliania huxleyi, calcifying strain CCMP 1516, which was the first coccolithophorid to have its genome sequenced by JGI (Read et al., 2013). The haptophytes significantly affect ocean biogeochemistry through their roles in the carbon and sulphur cycles. Emiliania huxleyi is a widely distributed species that typically blooms in high-latitude seas when and where the mixed layer is relatively shallow and thus characterized by high light (Iglesias-Rodriguez et al., 2002). Although its tolerance of high light is one of the attributes considered to contribute to blooms and the success of this species (Nanninga & Tyrrell, 1996), E. huxleyi can grow over a wide range of PFDs (Suggett et al., 2007). As in other photoautotrophs, growth of E. huxleyi in low light environments requires maximizing both the rate of light absorption per unit biomass and the quantum efficiency of photosynthesis, whilst tolerance of high light requires that oxidative stress and consequent cellular damage be minimized by reducing the production of ROS as well as increasing the scavenging of unavoidably produced ROS.
We investigated the functional consequences for light absorption, photosynthesis, nonphotochemical excitation energy quenching and photoinactivation that accompany the structural remodelling of the chloroplast proteome of E. huxleyi in response to growth at suboptimal and supraoptimal PFDs. We tested the hypotheses that changes in the efficiency of PSII photochemistry, the capacity for nonphotochemical quenching, and the susceptibility of RCII to photoinactivation could be explained as consequences of changes in the abundances of key chloroplast proteins. To this end, we used selected results from our analysis of the E. huxleyi proteomes under suboptimal and supraoptimal PFDs (McKew et al., 2013) together with new additional measurements of a suite of photophysiological characteristics. Unlike many previously published investigations, which focused on individual photophysiological processes in isolation, we have brought together observations of photoacclimation of light harvesting, nonphotochemical quenching and photoinactivation in conjunction with changes in the chloroplast proteome to assess the mechanistic basis of the cost–benefit trade-offs involved in photoacclimation.