Antenna proton sensitivity determines photosynthetic light harvesting strategy.

Eliška Kuthanová Trsková,Anna M Yeates,Roman Sobotka,Erica Belgio,Radek Kaňa,Alexander V Ruban

doi:10.1093/jxb/ery240

Abstract

Photoprotective non-photochemical quenching (NPQ) represents an effective way to dissipate the light energy absorbed in excess by most phototrophs. It is often claimed that NPQ formation/relaxation kinetics are determined by xanthophyll composition. We, however, found that, for the alveolate alga Chromera velia, this is not the case. In the present paper, we investigated the reasons for the constitutive high rate of quenching displayed by the alga by comparing its light harvesting strategies with those of a model phototroph, the land plant Spinacia oleracea. Experimental results and in silico studies support the idea that fast quenching is due not to xanthophylls, but to intrinsic properties of the Chromera light harvesting complex (CLH) protein, related to amino acid composition and protein folding. The pKa for CLH quenching was shifted by 0.5 units to a higher pH compared with higher plant antennas (light harvesting complex II; LHCII). We conclude that, whilst higher plant LHCIIs are better suited for light harvesting, CLHs are 'natural quenchers' ready to switch into a dissipative state. We propose that organisms with antenna proteins intrinsically more sensitive to protons, such as C. velia, carry a relatively high concentration of violaxanthin to improve their light harvesting. In contrast, higher plants need less violaxanthin per chlorophyll because LHCII proteins are more efficient light harvesters and instead require co-factors such as zeaxanthin and PsbS to accelerate and enhance quenching.

Highlights

It is often claimed that non-photochemical quenching (NPQ) formation/relaxation kinetics are determined by xanthophyll composition
Several processes contribute to excess light energy dissipation, but only the pH-dependent one, the Abbreviations: CLH, Chromera light harvesting complex; DCCD, dicyclohexylcarbodiimide; de-epoxidation state of the xanthophyll cycle pigments (DEPS), xanthophyll cycle de-epoxidation state; LHCII, light harvesting complex II; NPQ, non-photochemical quenching
We propose that protonation of the antenna is the basis of the ‘constitutively’ fast NPQ found in C. velia and, as previously suggested for diatoms (Lavaud and Kroth, 2006; Lavaud and Lepetit, 2013), ΔpH by itself is important for NPQ activation.This conclusion might explain the unusual high light acclimation strategy recently reported for C. velia, consisting of a decrease in reaction centers whilst still maintaining a full antenna content (Belgio et al, 2018)

Summary

Introduction

Under low light more than 83% of absorbed photons can be converted into chemical energy (e.g.Jennings et al.,2005; Wientjes et al, 2013), prolonged high light exposure rapidly switches photosystems to energy-dissipating states that release excess energy as heat (Demmig-Adams, 1990; Kaňa and Vass, 2008; Ruban et al, 2012). A very similar thermal dissipation process to that in vivo can be induced in vitro in purified antennas by lowering pH and detergent concentration (Ruban et al, 1994a) Starting from this evidence, it was proposed that antenna aggregation is at the basis of the NPQ process (Horton et al, 1996), and subsequent findings employing liposomes started to clarify how pH and ions together with lipids and lipid to antenna ratios control the ‘aggregation state’ of antennas (Moya et al, 2001; Kirchhoff et al, 2008; Akhtar et al, 2015; Kaňa and Govindjee, 2016; Natali et al, 2016; Crisafi and Pandit, 2017). Zeaxanthin, a highly hydrophobic pigment, in turn, makes antennas more dehydrated and sensitive to pH and prone to quench compared with violaxanthin-enriched antennas This idea was put forward for higher plant antennas (Ruban et al, 1994a), and for antennas from distant organisms such as diatoms (Gundermann and Büchel, 2008), brown algae (Ocampo-Alvarez et al, 2013) and alveolates (Kaňa et al, 2016)

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