High light intensity increases the concentrations of β-carotene and zeaxanthin in marine red macroalgae
Introduction
Light drives photosynthesis, but it may also may cause severe oxidative damage. Light capture fuels carbon fixation by providing ATP and NADPH. However, when carbon fixation is limited, for example, under stressful conditions, the captured light may become excessive, which would trigger the production of reactive oxygen species (ROS) [1,2]. Consequently, photosynthetic organisms have to regulate light harvesting to prevent the over excitation of chlorophyll. Intertidal macroalgae, which are mostly sessile on rock surfaces, periodically experience emersion and immersion in the course of diurnal tidal cycles. To survive such harsh environments, the light harvesting activities of intertidal macroalgae have to be controlled temporally during emersion, and then restored during immersion in seawater. The mechanisms modulating such modulation of light harvesting activities remain ambiguous.
To minimize the excitation of photosynthetic reaction centers under stress conditions, most photosynthetic organisms dissipate excessive light energy rapidly into harmless heat by inducing non-photochemical quenching (NPQ). NPQ has been reported to be modulated not only by pH-sensory membrane-binding peptides [3,4] but also by specific xanthophylls in plants and in most algae via the xanthophyll cycle [5]. When the captured light energy is excessive, the xanthophyll cycle is activated. According to the conformational model, the binding of xanthophyll that underwent de-epoxidation (zeaxanthin or diatoxanthin) to light harvesting complexes triggers the aggregation of light harvesting complexes of PSII (LHCII) facilitating the transformation of the captured light energy into heat, thereby minimizing the pressure induced by the high light conditions [6,7]. The unique properties involved in the control of the xanthophyll cycle in intertidal macroalgae have also been characterized [[8], [9], [10]]. However, the model can only be applied to higher plants and most algae that have trans-membrane LHCII. Red algae do not have hydrophobic LHCII, and mainly employ hydrophilic phycobilisomes as the major light harvesting antennae [11]. Therefore, the effects of zeaxanthin in inducing NPQ in red algae remain unclear.
Numerous studies have reported that zeaxanthin is present not only in green plants but also in cyanobacteria and red algae [12]. Recently, Tian et al. [13] reported high amounts of zeaxanthin in the light harvesting complex of PSI in a unicellular red alga, Cyanidioschyzon merolae. In addition, the key enzymes that catalyze the epoxidation of zeaxanthin (ZEP) have been observed in most red algae [14]; however, the key enzyme that converts violaxanthin to zeaxanthin is yet to be identified. Therefore, whether there is a functional xanthophyll cycle in red algae and the photoprotective role of zeaxanthin remain unclear.
Pyropia yezoensis is one of the most economically important intertidal red algae globally, and it exhibits remarkable tolerance to stress conditions based on photosynthetic activity [15,16]. Here, we report that the sporophytes of P. yezoensis accumulate zeaxanthin under relatively high light conditions, and the concentrations of the accumulated zeaxanthin did not reduce following transfer to conditions with relatively low light. In addition, high light conditions enhanced the transcriptional levels of the gene coding for β-carotene hydrogenase in P. yezoensis sporophytes. The results suggested that the accumulation of zeaxanthin in response to light stress was ubiquitous in oxygenic photosynthetic organisms.
Section snippets
Comparison of rapid light curves between Pyropia yezoensis sporophytes and gametophytes
P. yezoensis has a heteromorphic lifecycle including thallus (gametophyte) generation and conchocelis (sporophyte) generation. We compared their rapid light curves and the data are illustrated in Fig. 1. Gametophytes and sporophytes were cultured under similar light conditions in the laboratory. The rapid light curve (LC) data and the derivatives fitted from LC indicated that there were remarkable differences in PSII activities between the gametophytes and sporophytes of P. yezoensis. Notably,
Discussion
In the present study, we mainly investigated the responses of carotenoids to high light stress in P. yezoensis sporophytes. According to our results, the concentrations of β-carotene and the concentrations of its derivatives, i.e., zeaxanthin, were affected by environmental light conditions. When sporophytes were transferred to the high light conditions from the low light conditions, the concentrations of β-carotene and zeaxanthin increased substantially. The NPQ kinetics were also affected.
Cultivation of Pyropia yezoensis
P. yezoensis sporophytes and gametophytes were cultured in sterilized seawater at 16 ± 1 °C and illuminated with cool-white fluorescent lamps (light: dark = 12: 12). To investigate the effects of light intensity on photosynthetic capacity and lipid-soluble photosynthetic pigment concentrations, sporophytes were cultured under a series of light conditions by adjusting the distances between flasks and light tubes, i.e., 6 ± 2 μmolm−2 s−1, 15 ± 2 μmolm−2 s−1, 25 ± 2 μmolm−2 s−1, and 46 ± 2 μmolm−2
CRediT authorship contribution statement
Xiujun Xie:Conceptualization, Investigation, Formal analysis, Writing - original draft.Xiaoping Lu:Investigation, Formal analysis, Writing - original draft.Lepu Wang:Investigation, Formal analysis.Linwen He:Investigation, Formal analysis.Guangce Wang:Conceptualization, Writing - original draft.
Acknowledgements
This work was supported by the grant of Laboratory for Marine Biology and Biotechnology (OF2019NO07), Pilot National Laboratory for Marine Science and Technology (Qingdao), National Natural Science Foundation of China (41876160, 41806166, 41776149, 41506172, and 41776150), National Key Research and Development Program of China (2018YFD0901500), and Ministry of Agriculture and Rural Affairs of the People's Republic of China (CARS-50).
Declaration of competing interest
The authors declare that they have no conflicts of interest with the contents of this article, and no conflicts, informed consent, or human or animal rights are applicable to this study.
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These authors contributed equally.