Contrasting NPQ dynamics and xanthophyll cycling in a motile and a non‐motile intertidal benthic diatom

Abstract

Diatoms living in intertidal sediments have to be able to rapidly adjust photosynthesis in response to often pronounced changes in light intensity during tidal cycles and changes in weather conditions. Strategies to deal with oversaturating light conditions, however, differ between growth forms. Motile epipelic diatoms can migrate to more optimal light conditions. In contrast, non-motile epipsammic diatoms appear to mainly rely on higher Non-Photochemical Quenching (NPQ) of chlorophyll a fluorescence to dissipate excess light energy, and this has been related to a larger pool of xanthophyll cycle (XC) pigments. We studied the effect of 1 h high Photosynthetically Available Radiation (PAR) (2000 lmol photons m 22 s 21 ) on the kinetics of the xanthophyll cycle and NPQ in both a motile diatom (Seminavis robusta) and a non-motile diatom (Opephora guenter-grassii) in an experimental set-up which did not allow for vertical migration. O. guenter-grassii could rapidly switch NPQ on and off by relying on fast XC kinetics. This species also demonstrated high de novo synthesis of xanthophylls within a relatively short period of time (1 h), including significant amounts of zeaxanthin, a feature not observed before in other diatoms. In contrast, S. robusta showed slower NPQ and associated XC kinetics, partly relying on NPQ conferred by de novo synthetized diatoxanthin molecules and synthesis of Light-Harvesting Complex X (LHCX) isoforms. Part of this observed NPQ increase, however, is sustained quenching (NPQs). Our data illustrate the high and diverse adaptive capacity of microalgal growth forms to maximize photosynthesis in dynamic light environments.

Diversity in Xanthophyll Cycle Pigments Content and Related Nonphotochemical Quenching (NPQ) Among Microalgae: Implications for Growth Strategy and Ecology

“…, Blommaert et al. ), and ii) sea‐ice for a microalgal community dominated by diatoms ( Detonula confervacea , slope of 2.03; Katayama and Taguchi ) which are exposed to subzero temperatures, very high salinity and potentially moderate irradiances when the snow cover starts to melt in spring. High QEs of ca.…”

“…15 to 45 min on, depending on the species; see Blommaert et al. for the most recent example). This feature, as well as the lower QE under high light acclimation, have been attributed to the synthesis of additional Dt molecules that do not bind to the LHC system, and therefore, do not participate to NPQ (Schumann et al.…”

“…In Dd‐containing algae, the violaxanthin cycle can also be observed depending on species and light conditions (Lohr and Wilhelm , Blommaert et al. ). The violaxanthin cycle consists of two de‐epoxidation steps in which V is sequentially converted into anteraxanthin (A) and zeaxanthin (Z).…”

Light Regulation of LHCX Genes in the Benthic Diatom Seminavis robusta

“…The capacity for flexible NPQ is mainly defined by the xanthophyll cycle (XC) pigment diatoxanthin (Dtx) produced via de-epoxidation of diadinoxanthin (Ddx) (Lavaud and Goss, 2014;Barnett et al, 2015;Goss and Lepetit, 2015;Blommaert et al, 2017), and the presence of Light-Harvesting Complex X (LHCX) proteins (Bailleul et al, 2010;Ghazaryan et al, 2016;Taddei et al, 2016Taddei et al, , 2018Lepetit et al, 2017). While the XC in benthic diatoms has been well-studied in natural communities (van Leeuwe et al, 2008;Jesus et al, 2009;Serôdio et al, 2012;Laviale et al, 2015) and more recently also using unialgal isolates Blommaert et al, 2017), our current knowledge about LHCX proteins as an NPQ regulator is mostly based on studies of planktonic diatoms (Nymark et al, 2009(Nymark et al, , 2013Büchel, 2014;Lavaud and Goss, 2014;Valle et al, 2014;Dong et al, 2015;Goss and Lepetit, 2015;Ghazaryan et al, 2016;Grouneva et al, 2016;Lepetit et al, 2017;Taddei et al, 2018Taddei et al, , 2016. The latter includes studies on the pennate model diatom Phaeodactylum tricornutum which to date has only been isolated from water samples from various coastal environments, but may have a benthic growth phase as well (De Martino et al, 2007).…”

“…Recent studies using immuno-blotting revealed the presence of several light-regulated LHCX-proteins in natural communities and isolates of the microphytobenthic diatom S. robusta, of which some differ in size from P. tricornutum homologs Blommaert et al, 2017). To date, however, nothing is known about the diversity, organization and transcriptional regulation of these LHCX proteins in truly benthic diatoms.…”