Contrasting nonphotochemical quenching patterns under high light and darkness aligns with light niche occupancy in Arctic diatoms

Abstract

Over the seasons, Arctic diatom species occupy shifting habitats defined by contrasting light climates, constrained by snow and ice cover dynamics interacting with extreme photoperiod and solar angle variations. How Arctic diatom photoadaptation strategies differ across their heterogeneous light niches remains a poorly documented but crucial missing link to anticipate Arctic Ocean responses to shrinking sea-ice and increasing light. To address this question, we selected five Arctic diatom species with diverse life traits, representative of distinct light niches across the seasonal light environment continuum: from snow-covered dimly lit bottom ice to summer stratified waters. We studied their photoacclimation plasticity to two growth light levels and the subsequent responses of their nonphotochemical quenching (NPQ) and xanthophyll cycle to both dark incubations and light shifts. We deciphered NPQ and xanthophyll cycle tuning in darkness and their light-dependent induction kinetics, which aligned with species' light niche occupancy. In ice-related species, NPQ was sustained in darkness and its induction was more reactive to moderate light shifts. Open-water species triggered strong NPQ induction in darkness and reached higher maximal NPQ under high light. Marginal ice zone species showed strong adaptation to light fluctuations with a dark response fine-tuned depending upon light history. We argue these traits are anchored in diverging photoadaption strategies fostering Arctic diatom success in their respective light niches.

Divergence of photosynthetic strategies amongst marine diatoms

“…Interestingly, the strategies used to deal with dynamic high light are quite different within niche-specific diatom groups, whereby non-motile benthic diatoms employ rapidly reversible nonphotochemical quenching through XC-presumably to cope with more variable light fields [8,40]-whereas motile benthic diatoms preferentially employ slower, sustained non-photochemical quenching [21,29]. This pattern has been further confirmed comparing Artic diatoms [41]. Within pelagic species, the coastal taxon Skeletonema costatum exhibits inherently less capacity for sustained nonphotochemical quenching than the estuarine taxon Phaeodactylum tricornutum, but these alternate managements of excitation pressures are compensated by different capacities for PSII repair [42].…”

“…Diatoms exhibit varying responses to light to thrive across diverse environmental niches [40,41,101,[104][105][106]. Estuarine diatoms (e.g.…”

“…Sustained nonphotochemical quenching has been observed to have a linear relationship with Dt whereby at lower acclimated growth irradiances sustained nonphotochemical quenching at the initial dark fluorescence measure was around 5-fold lower than in high-light acclimated T. gravida [38]. However, recent studies have observed a deviation from this linearity [41], supporting the hypothesis that some portion of Dt is not directly related to nonphotochemical quenching and prevents full relaxation of nonphotochemical quenching [15]. While our study only obtained Dt concentrations at Ig and a brief (10 min) transient shift to HL, we cannot rule out the effect of Dt on sustained nonphotochemical quenching, and thus fluorescence signals retrieved.…”

Photosynthesis and photoprotection characteristics related to ROS production in three Chattonella (Raphidophyceae) species

“…According to our results, competition for light and the response to light stress conditions must also play an important role in the interaction between these phytoplankton groups. Chattonella can be considered as high-light specialist and a bad competitor for this resource and diatoms perform better under low-light conditions and can respond faster to changes in light conditions (Lavaud et al 2007, Croteau et al 2020). Therefore, Chatonnella can proliferate in high-light (low phytoplankton biomass) stratified environments.…”

Low-Cost Chlorophyll Fluorescence Imaging for Stress Detection

“…In the second study, we determined whether our CFI system can visualize downregulation of NPQ after a plant that was exposed to relatively high light conditions is transferred to darkness. This typically results in downregulation of NPQ [ 35 , 36 , 37 ] and we therefore hypothesized that this would be accompanied by an increase in chlorophyll fluorescence.…”