Photosynthesis acclimation under severely fluctuating light conditions allows faster growth of diatoms compared with dinoflagellates

Abstract

Background Diatoms contribute 20% of the global primary production and are adaptable in dynamic environments. Diatoms always bloom earlier in the annual phytoplankton succession instead of dinoflagellates. However, how diatoms acclimate to a dynamic environment, especially under changing light conditions, remains unclear. Results We compared the growth and photosynthesis under fluctuating light conditions of red tide diatom Skeletonema costatum, red tide dinoflagellate Amphidinium carterae, Prorocentrum donghaiense, Karenia mikimotoi, model diatom Phaeodactylum tricornutum, Thalassiosira pseudonana and model dinoflagellate Dinophycae Symbiodinium. Diatoms grew faster and maintained a consistently higher level of photosynthesis. Diatoms were sensitive to the specific inhibitor of Proton Gradient Regulation 5 (PGR5) depending photosynthetic electron flow, which is a crucial mechanism to protect their photosynthetic apparatus under fluctuating light. In contrast, the dinoflagellates were not sensitive to this inhibitor. Therefore, we investigate how PGR5 functions under light fluctuations in the model diatom P. tricornutum by knocking down and overexpressing PGR5. Overexpression of PGR5 reduced the photosystem I acceptor side limitation (Y (NA)) and increased growth rate under severely fluctuating light in contrast to the knockdown of PGR5. Conclusion Diatoms acclimatize to fluctuating light conditions better than dinoflagellates. PGR5 in diatoms can regulate their photosynthetic electron flow and accelerate their growth under severe light fluctuation, supporting fast biomass accumulation under dynamic environments in pioneer blooms.

Here comes the sun: How optimization of photosynthetic light reactions can boost crop yields

“…However, although overexpression of PGR5 in Flaveria bidentis led to alleviation of PSI acceptor side limitation, it did not result in enhanced CO 2 fixation (Munekage et al, 2010; Tazoe et al, 2020). In contrast, overexpression of PGR5 resulted in increased growth rates in diatoms under fluctuating light (Zhou et al, 2021) and enhanced high light and drought stress in Arabidopsis (Long et al, 2008). In addition, PTOX is also important as an alternative electron sink and for chloroplast biogenesis and carotenoid biosynthesis during early leaf development, and induction of its expression under stress conditions (summarized in Sun and Wen, 2011 and Johnson and Stepien, 2016; Ivanov et al, 2012; Li et al, 2016a; Ghotbi‐Ravandi et al, 2019) led to the suggestion that it could be a suitable target for enhancing stress tolerance in plants (Johnson and Stepien, 2016).…”

Flow cytometry-based study of model marine microalgal consortia revealed an ecological advantage of siderophore utilization by the dinoflagellate Amphidinium carterae

“…The different responses of NPQ regulation to iron could reflect the different general light response flexibilities of both species. In their natural environment, bloom-forming dinoflagellates live in a stable stratified layer at the subsurface, usually below approximately 10 m depth, where illumination can sometimes be reduced to 1% [23] . As a result, A. carterae is genotypically adapted to low quantum flux densities and lacks an effective mechanism for de-excitation when excess light is absorbed [24] .…”

“…As a result, A. carterae is genotypically adapted to low quantum flux densities and lacks an effective mechanism for de-excitation when excess light is absorbed [24] . On the other hand, planktonic diatoms, inhabiting turbulent surface waters, acclimatize to fluctuating light conditions better than dinoflagellates [23] . Diatoms are well known for their general light-response flexibility and potential for tuning their photosynthetic efficiency by NPQ under prolonged and potentially unfavorable conditions (reviewed in [25] ).…”

Mixoplankton interferences in dilution grazing experiments

“…1 h between the preparation of the experimental suspension of organisms and the collection of the initial sample. As such, we avoided the typical hunger response and consequent vacuole replenishment of starved predators 42 , and diminished the consequences of photoacclimation in the chlorophyll content of the phototrophs, as this is an almost immediate process 68 , 69 . The sampling occasions were the only sources of culture vessel mixing during the incubation.…”