Abstract

AbstractOver 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.

Highlights

  • We propose a strong evolutionary driving role of the sea-ice cover in promoting contrasted nonphotochemical quenching (NPQ) and xanthophyll cycle patterns, embedded in a survivalist photoadaptation strategy in sympagic diatom species as opposed to a more dynamic competition-oriented strategy of open-water planktonic diatoms

  • Photosynthetic, NPQ, and xanthophyll cycle (XC) parameters derived by fitting nonsequential light curves as described in Serôdio and Lavaud (2011)

  • NPQ and the underlying xanthophyll cycle are keystone components of species-specific photoadaptative strategies in most microalgae groups (Lacour et al 2020), allowing them to cope with changing light conditions and deeply influencing the global carbon cycle (Alvarez et al 2019)

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Summary

Introduction

In Baffin Bay, the productive season begins early in spring within the bottom centimeters of the snow-covered sea-ice (Habitat 1, Fig. 1), under extremely weak irradiances (Hancke et al 2018) Pennate diatoms dominate this sympagic biomass, frequently with major contributions from Nitzschia frigida (Poulin et al 2011). The molecular toolkit evolved by photoautotrophs to optimize growth in a specific light niche represents their photoadaptation strategy It comprises: (1) Day to season scale photoacclimative processes operating over generational time scales, including large modulations of light harvesting pigments and assimilatory enzymes like Rubisco in polar diatoms (Lacour et al 2017); and (2) Faster responding (seconds to hours) photoprotective mechanisms dissipating excessive light energy and mitigating photodamage. The central NPQ component is qE (“energy-dependent” quenching) whose dynamic regulation relies upon synergistic interactions between a transthylakoidal proton gradient, Fig. 1)

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