Protoplasmic streaming of chloroplasts enables rapid photoacclimation in large diatoms

Abstract

Long-term (2004–2020) studies showed yearly summer/autumn blooms in the NE Black Sea dominated by large (cell volume > 5000 μm3) diatoms (Pseudosolenia calcar-avis and Proboscia alata). This phenomenon is characterized by high (>250 W m−2 photosynthetically active radiation, PAR) insolation, and low phosphorus concentrations (to analytical zero). These diatoms contained >100 chloroplasts per cell, which at low irradiance are evenly distributed throughout the cell. As light increases (to 1000 μmol photons m−2 s−1 PAR), chloroplasts aggregate within 20 min, usually to the center of the cell. In consequence, the light absorption coefficient is decreased by >3 fold. At elevated photon flux density (PFD), P. calcar-avis also shows a “conveyor” of chloroplasts moving from the aggregate to the cell periphery and back. This mechanism enables a continuous fine-tuning of the cells’ ability to absorb light, likely also facilitating photo-damage repair. This rapid photoacclimation mechanism allows large diatoms to minimize photodamage at high PFD and acclimate well to low PFD. We hypothesize that competitive success of large diatoms in conditions of high light gradients is aided by this short-term rapid photoacclimation enhancing growth rate while minimizing chloroplast repair costs, aided by the ability of large cells to accumulate nutrients for chloroplast synthesis.

Phytoplankton Dynamics and Biogeochemistry of the Black Sea

“…In other words, a rapid growth strategy is implemented in this case [68]. The maximum specific growth rate is characteristic of small diatoms due to the high specific light absorption coefficients, which are several times higher than the same indicator for large diatoms [109]. Comparing Figure 5 we obtained with Figure 1 in the article by Meunier et al (2017), it should be noted that there is a significant difference.…”

Effect of a cyclonic eddy on phytoplankton: A bioassay experiment

“…Thus, based on the experimental results, it can be assumed that a typical Black Sea cyclonic eddy, lifting both the nutricline and thermocline, creates conditions close to optimal for this species. The physiological properties of this species, including the ability for rapid photoadaptation and storage of nutrients in a large vacuole (Silkin et al, 2021;Stelmakh, 2022), allow it to grow rapidly, using the increased flow of deep nutrients. The mass development of P. calcar-avis, observed in autumn in mesoscale cyclonic eddies of the Black Sea, confirms this assumption (Mikaelyan et al, 2018(Mikaelyan et al, , 2020.…”

“…These medium‐ and large‐celled species have regularly developed in the Black Sea (Mikaelyan et al., 2018). It has been shown that P. calcar‐avis can rapidly photoacclimate to low and high light due to the repackaging of chloroplasts (Silkin et al., 2021). This mechanism allows P. calcar‐avis to avoid photodegradation of pigments at the surface and deploy a photosynthetic antenna at a depth, which determines their ability to form blooms in the UML and the thermocline (Mikaelyan et al., 2021).…”

Annual Dynamics of Phytoplankton in the Black Sea in Relation to Wind Exposure

“…In a dynamic environment with a deep thermocline, the light intensity varies widely from photoinhibition level in the near-surface layer of water to light limitation at the ST lower boundary. According to another hypothesis, large diatoms can change the specific light absorption coefficient due to moving chloroplasts [12]. This ability allows them to change the amount of energy absorbed depending on the intensity of the light.…”

“…The classical concepts of regulating the annual dynamics of phytoplankton are based on the change of mixing regimes in the ocean and the associated vertical transport of nutrients [11]. Light intensity can also shift the structure of phytoplankton [12].…”