Shifts in growth light optima among diatom species support their succession during the spring bloom in the Arctic

Abstract

Diatoms of the Arctic Ocean annually experience extreme changes of light environment linked to photoperiodic cycles and seasonal variations of the snow and sea‐ice cover extent and thickness which attenuate light penetration in the water column. Arctic diatom communities exploit this complex seasonal dynamic through a well‐documented species succession during spring, beginning in sea‐ice and culminating in massive phytoplankton blooms underneath sea‐ice and in the marginal ice zone. The pattern of diatom taxa sequentially dominating this succession is relatively well conserved interannually, and taxonomic shifts seem to align with habitat transitions. To understand whether differential photoadaptation strategies among diatom taxa explain these recurring succession sequences, we coupled laboratory experiments with field work in Baffin Bay at 67.5°N. Based on field data, we selected five diatom species typical of different ecological niches and measured their growth rates under light intensity ranges representative of their natural habitats. To characterize their photoacclimative responses, we sampled pigments and total particulate carbon, and conducted 14C‐uptake photosynthesis response curves and variable fluorescence measurements. We documented a gradient in species respective light intensity for maximal growth suggesting divergent light response plasticity, which for the most part align with species sequential dominance. Other photophysiological parameters supported this ecophysiological framing, although contrasts were always clear only between succession endmembers, Nitzschia frigida and Chaetoceros neogracilis. To validate that these photoacclimative responses are representative of in situ dynamics, we compared them to the chlorophyll a‐specific light‐limited slope (α*) and saturated rate of photosynthesis (PM*), monitored in Baffin Bay on sea‐ice and planktonic communities. This complementary approach confirmed that unusual responses in α* and PM* as a function of light history intensity are similar between sentinel sympagic species N. frigida and natural ice‐core communities. While no light‐history‐dependent trends were observed in planktonic communities, their α* and PM* values were in the range of measurements from our monospecific cultures. Synthesis. Our results suggest that Arctic diatoms species photoadaptation strategy is tuned to the light environment of the habitats in which they dominate and indeed drives the seasonal taxonomic succession.

Potential for the Production of Carotenoids of Interest in the Polar Diatom Fragilariopsis cylindrus

“…In our study, a PUR of 11.7 µmol photons m −2 s −1 translates into a PAR of 30 µmol photons m −2 s −1 when ‘white’ light is used, which matches the light optimum of F. cylindrus [ 52 , 53 ]. Lowering the PUR to 5.4 µmol photons m −2 s −1 under both ‘white’ and blue lights for the same photoperiod (12 h L:12 h D) led to a lower growth rate accompanied by a decrease in photosynthesis (rETR max , α, E k , E opt ), an increase in light harvesting pigments (Chl a and Fx cell contents), and no change in the dark-acclimated photochemical efficiency (F V /F M ) and NPQ gE , which is a typical photoacclimatory response to a non-saturating light intensity in polar diatoms [ 27 , 53 , 60 , 61 , 62 ].…”

“…In a first step, we investigated the Fx and Ddx+Dtx cell contents and productivity of Fragilariopsis cylindrus grown in semi-continuous mode at 0 °C across a range of photoperiods with the same light intensity (30 µmol photons m −2 s −1 of photosynthetically available radiation (PAR), i.e., the optimal irradiance for F. cylindrus growth [ 52 , 53 ] and ‘white’ light spectrum (which reproduces the bottom ice light spectrum at best, see Figure S1 ) ( Figure 2 ). While the growth rate increased as a function of photoperiod length up to around 0.25 day −1 for a 18 h daylength and thereafter was saturated, F V /F M remained between 0.62 and 0.66 regardless of the photoperiod ( Figure 2 a).…”

“…Fact 1: the 0 °C temperature at which the experiments were performed, i.e., cold adaptation in polar diatoms was proposed to rely on similar physiological processes as high light acclimation [ 49 ] as in other photosynthetic organisms [ 75 ]. Fact 2: F. cylindrus is usually found to be abundant at the sea-ice bottom horizon and underneath ice [ 51 , 53 ], where red wavelengths are largely attenuated [ 43 , 44 ], and thus a 12 h monochromatic red light exposure per day during several weeks might have triggered the dramatic response we report. Fact 3: red light does not occur alone without a significant amount of blue-green light in the natural habitat of F. cylindrus , and the lack of blue light, especially, could be partly responsible for its poor performance under monochromatic red light.…”

“…The higher light conditions we tested with the same photoperiod (23.4 µmol photons m −2 s −1 PUR) exceeded the optimal growth light intensity of F. cylindrus at 0 °C [ 53 ]. In order to optimise the light energy usage and to maintain the same growth rate, F. cylindrus responded by lowering its light harvesting capacity (decrease in the Chl a and Fx contents), and photochemical efficency under light limitation (α), and increasing its capacity for dissipating the excess light energy (doubling of NPQ gE , increase in NPQ max, and Y NPQ ), which partially resulted in the decrease in their photosynthetic efficiency (F V /F M , rETR max ).…”

“…Interestingly, when comparing blue and ‘white’ light treatments of the same PUR (5.8 and 11.7 µmol photons m −2 s −1 PUR), we did not observe (apart from a consistent but not significant increase in NPQ) the blue light-triggered high-light acclimation previously described in temperate diatoms [ 38 , 63 ] and shown to be controlled by the aureochrome blue light photoreceptor family [ 64 , 65 ], although F. cylindrus does possess aureochromes [ 66 ]. F. cylindrus is usually found to be abundant at the sea-ice bottom horizon and underneath ice [ 51 , 53 ] where blue wavelengths dominate [ 43 , 44 ]. We propose that the apparent absence of this specific blue light response could be due to a differential sensitivity to blue light as compared to the planktonic temperate diatom species examined before [ 38 , 63 ].…”