The Peculiar Features of Non-Photochemical Fluorescence Quenching in Diatoms and Brown Algae

Abstract

International audienceDiatoms and brown algae are major contributors to marine primary production. They arebiologically diverse, with thousands of different species, and are extremely successful, occupyingalmost every marine ecosystem ranging from the coastal-estuarine to deep-sea regions.Their ecological success is based in part on their ability to rapidly regulate photosynthesis inresponse to pronounced fluctuations in their natural light environment. Regulation of light excessive energy as heat. Thermal dissipation of excitation energy is assessed as non-photochemicalquenching of chlorophyll a fluorescence (NPQ). NPQ depends strongly on theconversion of xanthophylls: diadinoxanthin (Dd) to diatoxanthin (Dt) in the Dd-Dt cycle ofdiatoms and violaxanthin (V) to zeaxanthin (Z), via the intermediate antheraxanthin (A), inthe VAZ cycle present in brown algae. Xanthophyll cycle (XC)-dependent thermal energydissipation underlying NPQ represents one of the most important photoprotection mechanismsof diatoms and brown algae. In the present chapter, we review the biochemistry of XCenzymes with a special focus on co-substrate requirements and regulation of enzyme activity.In addition, we present a new model for the structural basis of XC-dependent NPQ indiatoms based on the latest experimental findings. In the last section, we highlight the importanceof XC-dependent photoprotection for the ecological success of diatoms and brownalgae in their natural environments

Photosystem II repair in marine diatoms with contrasting photophysiologies

“…3c), both during and subsequent to HL incubation. These patterns are consistent with the studies showing induction of sustained quenching centers under prolonged HL exposure in P. tricornutum (i.e., persistence of a higher number of Q1 NPQ sites due to the persistence of DT molecules in the PSII LHC antenna) (see Lavaud and Goss 2014).…”

“…By significantly contributing to the cellular response under fluctuating light conditions (Wagner et al 2006;Mills et al 2010;Giovagnetti et al 2014), NPQ is critical for maintaining the photosynthetic efficiency of both planktonic and benthic diatoms (Lavaud and Goss 2014;Barnett et al 2015;Laviale et al 2015). An increasing number of reports suggest that diatom/microalgal interspecies differences in NPQ are involved in the differential colonization of marine habitats based on the light climate combined or not with other environmental factors including nutrients, temperature, and salinity (Strzepek and Harrison 2004;Lavaud et al 2007;Dimier et al 2007;Kropuenske et al 2009;Bailleul et al 2010;Mills et al 2010;Petrou et al 2011;van de Poll et al 2011;Wu et al 2012;Lavaud and Lepetit 2013;Barnett et al 2015;Juneau et al 2015).…”

“…They may (1) actively escape from excess light through motility, at least in benthic motile diatoms that inhabit the sediments of intertidal flats, (2) safely dissipate the excess of absorbed light energy, (3) balance the excess excitation energy within the photosynthetic apparatus and plastid, (4) scavenge reactive oxygen species, and (5) repair damage to proteins, thus containing and countering net photodamage to the photosynthetic and plastid machinery. In diatoms, one of these regulatory processes, believed to be essential, is the fast (i.e., seconds-scale timing) development of a thermal dissipation of excess energy that can be detected, thanks to a non-photochemical quenching of chlorophyll a (Chl a) fluorescence (NPQ) (Büchel 2014;Lavaud and Goss 2014). In diatoms, NPQ is controlled by (i) the lightdependent build-up of the transthylakoidal proton gradient (DpH), (ii) the DpH-dependent conversion of the xanthophylls diadinoxanthin (DD) into diatoxanthin (DT) called 'xanthophyll cycle' (XC) (Brunet and Lavaud 2010;Lavaud and Goss 2014), and (iii) the presence of specific polypeptides of the light-harvesting complex (LHC) antenna named Lhcx (Depauw et al 2012;Büchel 2014).…”

“…In diatoms, NPQ is controlled by (i) the lightdependent build-up of the transthylakoidal proton gradient (DpH), (ii) the DpH-dependent conversion of the xanthophylls diadinoxanthin (DD) into diatoxanthin (DT) called 'xanthophyll cycle' (XC) (Brunet and Lavaud 2010;Lavaud and Goss 2014), and (iii) the presence of specific polypeptides of the light-harvesting complex (LHC) antenna named Lhcx (Depauw et al 2012;Büchel 2014). Recently, a working mechanistic model for diatom NPQ has been proposed (see Chukhutsina et al 2014;Lavaud and Goss 2014;Derks et al 2015;Goss and Lepetit 2015) with two mechanistic and kinetic quenching components (namely Q1 and Q2).…”

“…In order to limit such situations, diatoms have evolved fast regulatory biological and physiological processes which comprise a 'photoprotective network' (Consalvey et al 2004;Lavaud and Goss 2014;Wilhelm et al 2014; Barnett et al 2015;Laviale et al 2015). They may (1) actively escape from excess light through motility, at least in benthic motile diatoms that inhabit the sediments of intertidal flats, (2) safely dissipate the excess of absorbed light energy, (3) balance the excess excitation energy within the photosynthetic apparatus and plastid, (4) scavenge reactive oxygen species, and (5) repair damage to proteins, thus containing and countering net photodamage to the photosynthetic and plastid machinery.…”