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

A Correction to this article was published on 30 April 2021

This article has been updated

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.

Peer Review reports

Background

Blooms during the upwelling season provide productivity in the ocean for a year and promote the global biochemical cycle [1, 2]. In early spring, pioneer diatoms bloom primarily from melting sea ice or sediment that was brought to the euphotic zone [3,4,5]. With diatom bloom recession, the matter and energy are converted to ocean sediment and subsequent blooms of dinoflagellates or zooplankton [3, 6,7,8]. However, the mechanism of the annual bloom succession between diatoms and dinoflagellates remains unclear.

Many studies along with analyses of monitoring data have been conducted to determine the imperative factor in the sequential bloom. A key reason for replacement of diatoms with dinoflagellates is nutrition [9,10,11]. Reduced dissolved silicate accelerates the decline of diatom biomass, and low nutrition increases the competitiveness of dinoflagellates [9,10,11,12,13]. Sufficient silicate is necessary (but not determinate) for the formation of diatom blooms [9, 14]. The temperature in late winter is also insufficient for diatoms to bloom in this season [2, 15, 16]. Some researchers have suggested that light [1, 2, 14,15,16,17] and wind [18,19,20] can be the stimuli for prolific diatoms, which needs further verification. However, these independent factors may not be applicable in all situations [14, 15, 21]. Therefore, to date, it is uncertain why diatom blooms form large-scale biomass in the short term and which factor signals the arrival of the blooms. Light fluctuation as a result of wind, turbulence, upwelling systems, waves, and surface lens effects [22,23,24] is an important environmental factor that has been monitored but ignored in ocean surveys [14, 15].

Notably, diatoms prefer and adapt to these dynamic environments, especially fluctuating light conditions. A temporarily enhanced wind can accelerate the growth of diatoms within a few days [18, 19]. In addition, diatoms are more adaptable in turbulent environments than dinoflagellates [3, 25, 26]. Reduced turbulence after stratification was considered a precondition of dinoflagellate bloom [25, 27]. Further, greater wave heights in winter and spring imply a more severe light fluctuation for diatoms. Pioneer diatoms are blown into shallow water, and blooms primarily occur within 50 m from the surface and could even concentrate on the surface [4, 12,13,14, 17, 28,29,30], whereas dinoflagellate blooms are usually in the subsurface, deeper than 10 m [1, 31,32,33]. The light intensity at the sea surface reaches 2000 μmol m− 2 s− 1 or sometimes more [14, 33, 34]. However, the illumination can sometimes be reduced to 1% at a depth of approximately 10 m [14, 15, 31, 33], especially for diatom blooms [14]. Finally, diatoms show absolute dominance in the upwelling system [35,36,37,38,39,40,41,42,43,44,45]. Diatoms can dominate in high-intensity upwelling regions and during upwelling stress periods [45,46,47]. In contrast, dinoflagellates are rich in stable regions and can only tolerate moderate and peripheral upwelling regions [40], an upwelling relaxation period [40, 45, 48, 49], or transitional period to downwelling [45, 50]. Besides nutrition and temperature, other more complex factors could influence the succession of diatom and dinoflagellate blooms. These special and changeable conditions imply that diatoms face complicated or multiple stresses, especially fluctuating light [14, 15].

Knowledge about the biological mechanism of bloom succession remains limited. Diatom was considered having special, efficient and well-adapted photosynthesis [51,52,53]. The fucoxanthin-Chl a/c complex (FCP), which was unique in diatom, can efficiently harvest light energy under low light and dissipate excess energy under high light [54]. However only few studies have focused on how these ocean photosynthetic organisms respond to light fluctuation [55]. In the current study, the growth and photosynthesis of three diatoms and four dinoflagellates under mildly fluctuating light (mFL) and severely fluctuating light (sFL) conditions were compared. The diatoms showed higher growth rates and more stable photosynthetic activity than the four dinoflagellates under the fluctuating light. The diatoms were also found to be sensitive to the inhibitor of Proton Gradient Regulation (PGR)5/PGRL1-dependent cyclic electron flow (CEF), a potential pathway responding to light fluctuations [56,57,58], whereas the dinoflagellates were not in this work.

Phaeodactylum tricornutum was used as a model to investigate how diatoms respond to fluctuating light in the ocean due to the availability of its complete genome sequence and pre-developed transformation techniques [59,60,61]. Overexpression of PGR5 could accelerate growth and decrease PSI accepted side limitations only under sFL, which was different from the findings of previous studies on photosynthesis in land and fresh water. Our results suggest that special photosynthesis in marine diatoms makes them grow better and acclimate to the turbulent sea surface and strong upwelling system.

Results

Growth and photosynthetic activities in marine diatoms and dinoflagellates under fluctuating light

The light environment of the seawater surface during the upwelling season was simulated, and the growth rates of the marine diatom P. tricornutum and the dinoflagellates P. donghaiense and K. mikimotoi, were compared. Under both mFL and sFL, the three diatoms grew faster than the four dinoflagellates (Fig. 1).

Fig. 1
figure1

Growth curves of red tide diatom S. costatum, red tide dinoflagellate A. carterae, P. donghaiense, and K. mikimotoi, model diatom P. tricornutum, T. pseudonana and model dinoflagellate D. Symbiodinium under a mFL after the addition of 1 min of bright light (800 μmol photons m− 2 s− 1) to every 5 min of low light (80 μmol photons m− 2 s− 1) and b sFL after the addition of 1 min of stronger light (2000 μmol photons m− 2 s− 1) to every 5 min of low light (20 μmol photons m− 2 s− 1). Culture experiments were repeated three times

To investigate the photosynthetic activities of these algae under dynamic light stress, PSI and PSII yields and related parameters were measured. Compared with those of the dinoflagellates, Y(I) and Y(II) of the diatoms showed smaller and more stable fluctuations with continuous conversion between strong and weak light. They also stayed active at a higher level when illuminated with sudden high light. After turning on the measured light, the Y(II) values of P. donghaiense and K. mikimotoi decreased rapidly and were less than 0.3 (Fig. 2). The Y(NA) of the three dinoflagellates increased erratically. Under mild light fluctuation, the Y(NA) values of the diatoms were lower than that of K. mikimotoi, whereas that of P. donghaiense was the lowest, although it had a high Y(ND) value (Fig. S1).

Fig. 2
figure2

a, b Chlorophyll and c, d P700 fluorescence of red tide diatom S. costatum, red tide dinoflagellate A. carterae, P. donghaiense, and K. mikimotoi, model diatom P. tricornutum, T. pseudonana and model dinoflagellate D. Symbiodinium under a, c mFL after the addition of 1 min of bright light (800 μmol photons m− 2 s− 1) to every 5 min of low light (80 μmol photons m− 2 s− 1). b, d sFL after the addition of 1 min of stronger light (2000 μmol photons m− 2 s− 1) to every 5 min of low light (20 μmol photons m− 2 s− 1). The experiments have three replicates

The fast kinetics of P700 was measured under the first SP after dark adaptation, and AA was used to inhibit the PGR5/PGRL1-regulated CEF pathway. The P700 in the diatoms maintained a high oxidation level during SP and was sensitive to AA (Fig. 3, S1).

Fig. 3
figure3

Fast kinetics of P700 during 300 ms SP after dark adaptation with or without 10 μM inhibitor Antimycin A (AA) in red tide diatom b S. costatum, red tide dinoflagellate d A. carterae, e P. donghaiense, and f K. mikimotoi, model diatom c P. tricornutum, a T. pseudonana and model dinoflagellate g D. Symbiodinium. Data was normalized to [0,1] using origin 9.0

Growth and photosynthetic parameters of PGR5 knocked down and overexpressing P. tricornutum under mFL and sFL

Since diatom was sensitive to the inhibitor AA, we used P. tricornutum, the model diatom with stable and efficient transformation methods, to investigate whether PGR5 in diatom responds to light fluctuation. Bioinformatics analysis revealed that the 61–132 base pair region that represents PGR5 in P. tricornutum is conserved, and the first 20 bases form a potential signal peptide, as determined using SignalP-3.0 (http://www.cbs.dtu.dk/services/SignalP-3.0/). The PGR5 of Chlorophyta, Rhodophyta, Phaeophyta, and diatoms were on the same evolutionary branch as that of Cyanobacteria, but those of terrestrial green plants were on another branch. The diatom PGR5 was found to be closer to Phaeophyta and Rhodophyta PGR5. A protein similar to PGR5 was found in the dinoflagellates. However, several conserved sites were missing, especially when compared with those in motif 1, and no homology with sequences in other plants and algae was observed (Fig. S2).

We constructed 5OE-1 and 5KN-i1 and verified them using PCR amplification, quantitative PCR, and western blot analysis. The silencing or overexpression effect in the selected algal strain was significant (Fig. S3). In each cultivation treatment, PGR5 overexpression and knockdown effects were maintained, but PGR5 expression was significantly higher under fluctuating light than under constant light (CL) condition.

The growth of P. tricornutum under fluctuating light was next investigated (Fig. 4). No differences were observed among the WT, 5OE-1, and 5KN-i1 under mFL. In contrast, under sFL, the growth rate of 5KN-i1 was significantly restricted, whereas that of 5OE-1 improved.

Fig. 4
figure4

Growth curves under a mFL after the addition of 1 min of bright light (800 μmol photons m− 2 s− 1) to every 5 min of low light (80 μmol photons m− 2 s− 1) and b sFL after the addition of 1 min of stronger light (2000 μmol photons m− 2 s− 1) to every 5 min of low light (20 μmol photons m− 2 s− 1). Culture experiments were repeated three times. The values shown are the means of three biological replicates

The photosynthetic parameters of the WT, 5OE-1, and 5KN-i1 under mFL and sFL were measured. The P700 parameters for mFL and sFL differed significantly (Fig. 5). Under mFL, the PSI yields of WT, 5OE-1, and 5KN-i1 were similar, except for that of 5KN-i1, which increased slightly under bright light owing to increased donor side limitation. However, under sFL, the PSI acceptor side of 5KN-i1 was severely restricted, but the limitation in 5OE-1 was low. The differences in Y(NA) values between bright light and low light and Y(ND) values between dim or dark conditions and bright light showed the same trend.

Fig. 5
figure5

Photosynthetic parameters for P700. a, c and e: under mFL after the addition of 1 min of bright light (dark yellow, 800 μmol photons m− 2 s− 1) to every 5 min of low light (white, 80 μmol photons m− 2 s− 1); b, d and f: under sFL after the addition of 1 min of stronger light (bright yellow, 2000 μmol photons m− 2 s− 1) to every 5 min of low light (gray, 20 μmol photons m− 2 s− 1). The values shown are the means of at least three biological replicates. a and b: Y(I), PSI yield; c and d: Y(NA), PSI acceptor side limitation; e and f: Y(ND), PSI donor side limitation

Other photosynthetic characteristics also showed large differences among WT, 5OE-1, and 5KN-i1 (Fig. 6). The 1-qL and NPQ of 5KN-i1 decreased under the bright light phase of FL, whereas the Y(II) in 5KN-i1 increased under the low light phase of FL. In contrast, under high light, NPQ and 1-qL increased in 5OE-1. Under sFL, the differences in NPQ among WT, 5OE-1, and 5KN-i1 were more apparent, although the values were smaller overall. However, the difference in 1-qL was smaller under sFL. The Y(II) values also differed in that the Y(II) of 5KN-i1 was highest under mFL but equal to that in WT and 5OE-1 under sFL. Furthermore, the 1-qL in 5KN-i1 increased when moving from dark to low light under mFL and decreased in 5OE-1.

Fig. 6
figure6

Photosynthetic parameters for PSII, a, c and e: under mFL after the addition of 1 min of bright light (dark yellow, 800 μmol photons m− 2 s− 1) to every 5 min of low light (white, 80 μmol photons m− 2 s− 1); and b, d and f: under sFL after the addition of 1 min of stronger light (bright yellow, 2000 μmol photons m− 2 s− 1) to every 5 min of low light (gray, 20 μmol photons m− 2 s− 1). The values shown are the means of at least three biological replicates. a and b: NPQ, non-photochemical quenching; c and d: Y(II), the actual conversion efficiency of light energy of PSII; e and f: 1 - qL, PQ redox state

Discussion

Diatoms demonstrate better acclimation to fluctuating light than dinoflagellates, supporting diatom dominance in pioneer bloom of phytoplankton succession

Many researchers have focused on the succession of marine phytoplankton blooms. They recognized that depletion of nutrients, especially silicate, can cause diatom bloom recession and subsequent dinoflagellate bloom [9,10,11]. However, the key factor in early diatom blooms is still disputed [1, 2, 13,14,15,16,17,18,19, 21]. Researchers have attempted to identify factors that improve competitiveness in pioneer blooms and support huge biomass increases over several days in diatoms [1, 18, 28, 62].

In addition to nutrition, temperature, wind, and light were also investigated and are considered influential in pioneer blooms. However, all these traditional factors are contradictory and were regionally restricted in some marine surveys. Although the scale of dinoflagellates expands with increasing nitrogen or phosphate content, it cannot replace the pioneer role of the diatom [63,64,65,66]. Dinoflagellates can bloom in winter or quickly follow diatom blooms [2, 67,68,69], whereas dinoflagellate cysts may sprout slowly due to low temperatures when diatoms bloom. Increased temperature has the opposite effect in promoting bloom time or increasing predation pressure [2]. Sometimes, wind can reduce blooms [2], and light appears to lose its effect on the bloom. In fact, the mean value of light intensity does not represent the actual light environment well. In addition to environmental influences, differences in acclimation and growth between diatoms and dinoflagellates are also important. It is suggested that the higher growth rate of diatoms is the key to early blooms [1, 15, 18, 28, 68, 70]. Recently, some studies have suggested that diatoms have strong adaptation and recovery ability in long, cold, dark periods, which supports the bloom in late winter [71,72,73]. In fact, adaptation to complex and dynamic environments is also important in the large-scale spring bloom due to strong, coastal upwelling and violent waves without stabilized stratification.

Therefore, the current study suggests that light fluctuation and better acclimation to fluctuating light in diatoms, in addition to what is traditionally known, can also be the reasons for diatom dominance in pioneer blooms (Fig. 7 [74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99]). though acclimation to dynamic light in photosynthetic organisms on land and in fresh water has been studied in the past few years, the key mechanisms in marine algae are still unknown. The dominance of diatoms in a dynamic environment suggests potential mechanisms for adapting to fluctuating light, which confers an advantage over dinoflagellates that prefer a stable environment. With sufficient nutrients and without temperature limitations, diatoms have more growth advantages in the short term than dinoflagellates under both mild and severe light fluctuations (Fig. 1), which could support the fast bloom and absolute dominance of diatoms in a strong upwelling system or on the turbulent sea surface.

Fig. 7
figure7

Traditional seasonal succession model of diatom and dinoflagellate blooms (not excluding the specificity of regional and annual differences and the impact of future climate change). The top part shows the distribution and environmental factors in diatom and dinoflagellate blooms. The bottom part lists currently known biological properties relative to the succession. The curve of dissolved silicon is referred to in previous work [10]. The graphic represents the monitored, decisive, non-biological factors in bloom succession (light, wind, and late silicate concentration) and the dotted line represents insufficient factors (temperature and early silicate concentration). Asterisk represents environmental factor associated to fluctuating light

Photosynthesis is a key physiological process that plays an important role in the growth response to dynamic environmental stresses [56] Diatoms demonstrate more effective photosynthesis and better resistance under light fluctuation conditions than dinoflagellates (Fig. 2). In dynamic changes between bright and low light, the PSI and PSII of diatoms were able to stabilize these fluctuations and maintain high levels of activity. Diatoms use sudden periods of bright light more efficiently (even when saturated with sunlight [14, 100]), resulting in higher actual PSII and PSI yields than those in dinoflagellates. Efficient photosynthesis even under saturated illumination could support the huge biomass and sufficient acclimation on the sea surface. Even under sFL, the diatoms maintain lower PSI acceptor limitation (Fig. S1), indicating that they can more efficiently regulate excess electrons under fluctuating light, which affords them a stronger ability to resist and use fluctuating light to adapt to strong periods and regions of upwelling.

These results imply that light fluctuation can influence on the competition between diatoms and dinoflagellates.

Photosynthesis can support rapid growth of pioneer diatoms under fluctuating light

The acclimation of photosynthesis to light fluctuations implies a molecular mechanism in diatoms that could promote growth. Diatoms were considered to lack FLV (an A-type flavoprotein), the key protein that acts in response to fluctuating light in freshwater algae [56, 101]. Notably, PGR5, another potentially critical protein in resisting light fluctuations, has been reported in the diatom proteome [120]. In this study, PGR5 was found to play an important role in the acclimation of diatoms to fluctuating light.

Antimycin A is an efficient and specific inhibitor of PGR5/PGRL1 depending on CEF. Previously, diatom CEF was measured to be low, and CEF (depending on PGR5/ PGRL1) was ignored in response to light fluctuation due to the moderate treatment [55]. Further, increased or decreased PGRL1 levels did not lead to enhancement of photosynthesis and growth in diatoms under fluctuating light [102]. The redox state of P700 was significantly lower after addition of AA to the diatoms than that in the dinoflagellates (Fig. 3), which implied that diatoms have a more effective CEF depending on PGR5/PGRL1, which is the key response to various light stresses. Although dinoflagellates contain the PGR5 homologous gene, it has no or negligible function, presumably due to abundant transferring genes in the mesokaryotic genome, a possible fusion gene with PGRL1 [103], or the minimally conserved C-terminal sequence (Fig. S2).

In the current study, PGR5 protein levels improved both photosynthetic electron flow and growth rate under sFL (between very low light [15] and saturated with sunlight [15, 100]). No significant growth differences were found under mild light fluctuation in 5KN-i1, WT, and 5OE-1 (Fig. 4a). However, under sFL, the growth rate of 5KN-i1 significantly decreased, whereas 5OE-1 grew rapidly. This implies that PGR5 in diatoms, which was underestimated previously, is sensitive to the intensity of light fluctuations. Photosynthesis showed the same result, especially in the acceptor side limitation of PSI [Y(NA)] (Fig. 5). In fact, PGR5 prevents PSI over-reduction on the acceptor side by increasing the production ratio of ATP/NADPH through ATP generation and electron transport for Cyt b6f or PQ. Compared with previous studies on the effect of dynamic light on terrestrial plants and freshwater algae, in this study, the special response to different light fluctuation intensities in the diatoms was associated with a preference for a concentrated bloom on the sea surface and a strong upwelling system. Indeed, diatoms always face frequent and large variations in light intensity due to shelter by high cell concentrations, wind agitation, and the surface lens effect. These results also reveal the crucial role of photosynthesis in diatom growth. Therefore, we suggest that the special acclimation mechanism of diatoms to fluctuating light might be imperative in their pioneering nature.

Conclusion

This work implied that light fluctuation is a crucial factor in phytoplankton succession in diatoms and dinoflagellates. Diatoms are better acclimatized to fluctuating light than dinoflagellates in both growth and photosynthesis. Thus, diatoms acclimatize better to the dynamic environment and have growth advance in pioneer bloom under stronger upwelling, wave and wind conditions. PGR5 in diatom plays crucial roles under severe light fluctuation, supporting the photosynthesis adaptability and growth under variable environments of diatom. The results will also supplement to the responding mechanism to dynamic light in ocean photosynthesis organisms.

Materials and methods

Strain, cultivation, and growth monitoring

The diatom Skeletonema costatum and dinoflagellates Amphidinium carterae, Prorocentrum donghaiense, and Karenia mikimotoi are red tide species, whereas the diatoms P. tricornutum and Thalassiosira pseudonana and the dinoflagellate Dinophycae Symbiodinium are model species. Seven algae were grown in sterile artificial seawater containing F/2 medium at a temperature of 21 ± 1 °C. The light/dark cycle was set to 12 h/12 h. Following previous study on fluctuating light [56, 57, 101], mFL condition ranged from 100 to 10% of the bright light below the tolerance level of dinoflagellates (Fig. 7) [104]. In details, a 1-min period of bright light (800 μmol m− 2 s− 1) was added to each 5 min of low light (80 μmol m− 2 s− 1) in the mFL treatment. The larger fluctuating extent and higher light intensity were brought in sFL condition that ranged from 100% [14, 33, 34] to 1% [14, 15, 33] of the saturated sunlight. A 1 min of stronger light (2000 μmol m− 2 s− 1) was added to each 5 min of lower light (20 μmol m− 2 s− 1) in the sFL treatment.

The cell densities of the algae were counted using a hemocytometer, and growth of the wild-type (WT), PGR5 overexpression algae (5OE-1), and pgr5 knockdown algae (5KN-i1) of P. tricornutum was measured based on the absorbance at 730 nm wavelength (UV-1800, SHIMADZU, Japan). During the middle exponential growth phase, all the algae strains were centrifuged and flash-frozen at − 80 °C.

Chlorophyll and P700 fluorescence parameter monitoring

During the exponential growth phase, the chlorophyll fluorescence parameters were monitored using a Dual-PAM-100 (Walz, Effeltrich, Germany) instrument with WinControl software 1 h after the beginning of the light cycle, under the same conditions used to culture the algae. The chlorophyll fluorescence and P700 were both measured using dual-channel equipment. The algae were kept in the dark for 10 min before measurement. Antimycin A (AA, 10 μM) was added when required [105]. The minimum fluorescence (F0), maximum fluorescence (Fm, after a saturating flash), and maximum fluorescence (Fm′, under photosynthetic active radiation) were measured and used to calculate the following values:

$$ \mathrm{Maximum}\ \mathrm{light}\ \mathrm{conversion}\ \mathrm{efficiency}:{\mathrm{F}}_{\mathrm{v}}/{\mathrm{F}}_{\mathrm{m}}=\left({\mathrm{F}}_{\mathrm{m}}-{\mathrm{F}}_0\right)/{\mathrm{F}}_{\mathrm{m}} $$
(1)

Effective PS II activity:

$$ \mathrm{Y}\left(\mathrm{II}\right)=\left(\mathrm{Fm}^{\prime }-\mathrm{F}\right)/\mathrm{Fm}^{\prime }, $$
(2)
$$ \mathrm{Non}-\mathrm{photochemical}\ \mathrm{quenching}:\mathrm{NPQ}=\left({\mathrm{F}}_{\mathrm{m}}-{\mathrm{F}}_{\mathrm{m}}\right)/{\mathrm{F}}_{\mathrm{m}}^{\prime }, $$
(3)

and Photochemical quenching coefficient:

$$ \mathrm{qL}=\left[\left({\mathrm{F}}_{\mathrm{m}}^{\prime }-\mathrm{F}\right)/\left({\mathrm{F}}_{\mathrm{m}}^{\prime }-{\mathrm{F}}_{\mathrm{o}}^{\prime}\right)\cdotp {\mathrm{F}}_{\mathrm{o}}^{\prime }/\mathrm{F}\right]. $$
(4)

Similarly, the maximum change in the P700 signal (Pm), maximum change in the P700 signal under photosynthetic active radiation (Pm′), zero P700 signal (P0), and the fraction of overall P700 reduction after the saturation pulse were used to calculate the photosystem I (PSI) donor side limitation (Y[ND]), acceptor side limitation (Y[NA]), and the PSI yield, using the following equation:

$$ \mathrm{Y}\left(\mathrm{I}\right)=1-\mathrm{Y}\left(\mathrm{ND}\right)-\mathrm{Y}\left(\mathrm{NA}\right) $$
(5)

Phylogenetic analysis and transformation

The PGR5 sequence in P. tricornutum (Gene ID: 7199723) was downloaded from the National Center for Biotechnology Information database. Protein sequences of other species were downloaded from the National Center for Biotechnology Information and UNIPROT databases. Similar sequences of PGR5 in dinoflagellates were identified using NCBI-BLAST [106] from the genome assembly (WGS Project: BASF01, BGNK01, BGPT01, GAFO01, GBSC01, GFLM01, GFPM01, GHKS01, GICE01, IADN01, IADM01, VSDK01) and RNA-seq of Prorocentrum donghaiense (Accession: PRJNA374496) [107,108,109,110,111,112,113,114,115,116]. MEGA 7.0 was used to construct a maximum likelihood evolutionary tree after alignment using ClustalW.

A 157 bp partial sequence containing motif 4 (which is predicted, using MEME suite 5.1.1 [117], to be unique to diatoms) and the 3′ untranslated region (UTR) of P. tricornutum were amplified, and the products were digested using HindIII (sense) and EcoRI (anti-sense). The sequence was inserted in reverse into the multiple cloning site of the pPha-T1 vector [118] (after FcpA promoter, a strong promoter resounding to light [119]) using EcoRI and HindIII restriction enzyme digestion for PGR5 knockdown in P. tricornutum. Vectors for PGR5 overexpression were generated by cloning the full-length PGR5 gene and inserting it in the forward direction.

Gold particles (50 μL/3 mg) with 20 μL spermidine (0.1 M), 50 μL CaCl2 (2.5 M) and 5 μg plasmids (approximately 10 μL) were used for transformation using particle bombardment (BIO-RAD Biolistic PDS-1000/H2 Particle Delivery System, CA, USA) [51, 61]. After 24 h of recovery under low light, the algae were transferred onto plates containing zeocin (100 μg/mL). After 20–30 days, individual algal colonies were retrieved and lysed for direct polymerase chain reaction (PCR) to verify sequence integration. The individual colonies were then cultured in liquid medium containing zeocin (100 μg/mL).

Real-time PCR analysis

Real-time PCR was used to verify that the target sequence had been integrated into the genome and to determine the PGR5 mRNA expression level (Fig. S3). RNA extraction and real-time PCR analysis were performed according to methods described by Wu et al. [105]. Total RNA was obtained from frozen algae using an RNA prep Pure Plant kit (polysaccharide and polyphenolic-rich) (Tiangen, Beijing, China). RNA quality was assessed using a NanoPhotometer (IMPLEN, Munich, Germany) and 1% agarose gel electrophoresis. Reverse transcription was performed using a PrimeScript RT reagent kit with gRNA Eraser (Takara, Beijing, China). The cDNA was used as a template and quantified via quantitative PCR, using a FastStart Essential DNA Green Master (Roche) in an iQ5 multicolor real-time PCR detection system (Bio-Rad, Hercules, USA) with Bio-Rad optical system software. The internal control was the RPS (ribosomal protein small subunit 30S) gene (Table S1).

Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and immunoblotting analysis

Protein levels were quantified using western blot analysis. Thylakoid membrane protein extraction was performed according to the method described by Grouneva et al. [120]. Frozen algae (collected from fresh algae approximately in the middle of their exponential growth period) were ground in liquid nitrogen and centrifuged at 300×g to remove cell debris and impurities after the addition of extraction buffer (10 mM MES, 2 mM KCl, 5 mM Na2EDTA, and 1 M D-sorbitol; pH 6.5). The sediment was ground again in extraction buffer and centrifuged at 300×g. All supernatants were collected and centrifuged at 20,000×g. The sediment was washed twice in lysis buffer (which was identical to the extraction buffer, except that it did not contain d-sorbitol) and then suspended in storage solution (25 mM Tris-HCl and 20% glycerol; pH 7.0). All solutions were pre-cooled at 4 °C, and the thylakoid membrane proteins were stored at − 80 °C. The chlorophyll and BCA methods (Fig. S3) were used to quantify the protein, and 5 μg of Chl or 50 μg of protein (for pigment change under different conditions) was analyzed using sodium dodecyl sulfate-polyacrylamide gel electrophoresis [121, 122]. Antibodies against PsaB (photosystem I P700 chlorophyll a apoprotein A2) and ATPB (ATP synthase subunit β, chloroplastic) were purchased from Agrisera (Vännäs, Sweden), and an antibody to PGR5 was produced in our laboratory (antigenic peptide sequence: TKLIKKAKVNGDTLGF).

Availability of data and materials

The datasets used and/or analyzed during the current study are available from corresponding authors on reasonable request. The sequences used in this work are available in NCBI database (http://www.ncbi.nlm.nih.gov) or UniProtKB/TrEMBL database (https://www.uniprot.org/). NCBI accession numbers are 330,250,863, 164,449,273, 1,387,830,212, 586,688,763, 196,168,724, 393,690,734, 357,144,276, 573,956,334, 1,435,170,242, 1,394,909,989, 1,373,914,553, 971,519,293, 1,331,346,858, 926,775,414, 675,355,490, 158,308,814, 219,867,356, 1,189,386,569, 1,395,913,517; UniProtKB/TrEMBL identifiers are I1ZIR9, A1YSQ5, D7G229, B8C035, B7FVH9; NCBI-Assembly accession numbers are BASF01, BGNK01, BGPT01, GAFO01, GBSC01, GFLM01, GFPM01, GHKS01, GICE01, IADN01, IADM01, VSDK01,PRJNA374496.

Change history

Abbreviations

PGR5:

Proton Gradient Regulation 5

mFL:

mildly fluctuating light

sFL:

severely fluctuating light

CL:

constant light

WT:

wild-type

5OE-1:

PGR5 overexpression algae

5KN-i1:

pgr5 knockdown algae

AA:

Antimycin A

CEF:

cyclic electron flow

FLV:

an A-type flavoprotein)

Y(I):

PSI yield

Y(NA):

PSI acceptor side limitation

Y(ND):

PSI donor side limitation

NPQ:

non-photochemical quenching

Y(II):

the actual conversion efficiency of light energy of PSII

1–qL:

PQ redox state

References

  1. 1.

    Strom SL, Fredrickson KA, Bright KJ. Spring phytoplankton in the eastern coastal Gulf of Alaska: photosynthesis and production during high and low bloom years. Deep-Sea Res Pt Ii. 2016;132:107–21.

    CAS  Google Scholar 

  2. 2.

    Hjerne O, Hajdu S, Larsson U, Downing AS, Winder M. Climate driven changes in timing, composition and magnitude of the Baltic Sea phytoplankton spring bloom. Front Mar Sci. 2019;6.

  3. 3.

    Treguer P, Bowler C, Moriceau B, Dutkiewicz S, Gehlen M, Aumont O, Bittner L, Dugdale R, Finkel Z, Iudicone D, et al. Influence of diatom diversity on the ocean biological carbon pump. Nat Geosci. 2018;11(1):27–37.

    CAS  Google Scholar 

  4. 4.

    Lafond A, Leblanc K, Queguiner B, Moriceau B, Leynaert A, Cornet V, Legras J, Ras J, Parenteau M, Garcia N, et al. Late spring bloom development of pelagic diatoms in Baffin Bay. Elementa-Sci Anthrop. 2019;7.

  5. 5.

    Dutkiewicz A, Muller RD, O'Callaghan S, Jonasson H. Census of seafloor sediments in the world's ocean. Geology. 2015;43(9):795–8.

    CAS  Google Scholar 

  6. 6.

    Liu Y, Zhao W, Li C, Miao H. Free polyamine content during algal bloom succession in the East China Sea in spring 2010. Chin J Oceanol Limnol. 2017;35(1):215–23.

    CAS  Google Scholar 

  7. 7.

    Zhang G, Liang S, Shi X, Han X. Dissolved organic nitrogen bioavailability indicated by amino acids during a diatom to dinoflagellate bloom succession in the Changjiang River estuary and its adjacent shelf. Mar Chem. 2015;176:83–95.

    CAS  Google Scholar 

  8. 8.

    Benoiston A-S, Ibarbalz FM, Bittner L, Guidi L, Jahn O, Dutkiewicz S, Bowler C. The evolution of diatoms and their biogeochemical functions. Philos Trans R Soc B. 2017;372(1728):20160397.

    Google Scholar 

  9. 9.

    Hutchins DA, Bruland KW. Iron-limited diatom growth and Si : N uptake ratios in a coastal upwelling regime. Nature. 1998;393(6685):561–4.

    CAS  Google Scholar 

  10. 10.

    Coffineau N, De La Rocha CL, Pondaven P. Exploring interacting influences on the silicon isotopic composition of the surface ocean: a case study from the Kerguelen plateau. Biogeosciences. 2014;11(5):1371–91.

    CAS  Google Scholar 

  11. 11.

    Zhang YQ, Lin X, Shi XG, Lin LX, Luo H, Li L, Lin SJ. Metatranscriptomic signatures associated with phytoplankton regime shift from diatom dominance to a Dinoflagellate bloom. Front Microbiol. 2019;10.

  12. 12.

    Allen JT, Brown L, Sanders R, Moore CM, Mustard A, Fielding S, Lucas M, Rixen M, Savidge G, Henson S, et al. Diatom carbon export enhanced by silicate upwelling in the Northeast Atlantic. Nature. 2005;437(7059):728–32.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Yoshie N, Yamanaka Y. Processes causing the temporal changes in Si/N ratios of nutrient consumptions and export flux during the spring diatom bloom. J Oceanogr. 2005;61(6):1059–73.

    CAS  Google Scholar 

  14. 14.

    Carvalho F, Fitzsimmons JN, Couto N, Waite N, Gorbunov M, Kohut J, Oliver MJ, Sherrell RM, Schofield O. Testing the canyon hypothesis: evaluating light and nutrient controls of phytoplankton growth in penguin foraging hotspots along the West Antarctic peninsula. Limnol Oceanogr. 2020;65(3):455–70.

    CAS  Google Scholar 

  15. 15.

    Rune ES. Ecological studies on the phytoplankton of Boknafjorden, western Norway. II Environmental control of photosynthesis. J Plankton Res. 1989;4:4.

    Google Scholar 

  16. 16.

    Mutshinda CM, Finkel ZV, Irwin AJ. Which environmental factors control phytoplankton populations? A Bayesian variable selection approach. Ecol Model. 2013;269:1–8.

    Google Scholar 

  17. 17.

    Peeters JCH, Haas H, Peperzak L, Wetsteyn LPMJ. Limiting factors for phytoplankton in the North Sea. Water Sci Technol. 1991;24(10):261–7.

    Google Scholar 

  18. 18.

    Iluz D, Dishon G, Capuzzo E, Meeder E, Astoreca R, Montecino V, Znachor P, Ediger D, Marra J. Short-term variability in primary productivity during a wind-driven diatom bloom in the Gulf of Eilat (Aqaba). Aquat Microb Ecol. 2009;56(2–3):205–15.

    Google Scholar 

  19. 19.

    Sorooshian A, Padro LT, Nenes A, Feingold G, McComiskey A, Hersey SP, Gates H, Jonsson HH, Miller SD, Stephens GL, et al. On the link between ocean biota emissions, aerosol, and maritime clouds: airborne, ground, and satellite measurements off the coast of California. Global Biogeochem Cy. 2009;23.

  20. 20.

    Kiorboe T, Lundsgaard C, Olesen M, Hansen JLS. Aggregation and sedimentation processes during a spring phytoplankton bloom - a field experiment to test coagulation theory. J Mar Res. 1994;52(2):297–323.

    Google Scholar 

  21. 21.

    Alderkamp A-C, van Dijken G, Lowry K, Connelly T, Lagerström M, Sherrell R, Haskins C, Rogalsky E, Schofield O, Stammerjohn S, et al. Fe availability drives phytoplankton photosynthesis rates during spring bloom in the Amundsen Sea Polynya, Antarctica. Elementa. 2015;3:000043.

    Google Scholar 

  22. 22.

    Leeuwe MAV, Sikkelerus BV, Gieskes WWC. Taxon-specific differences in photoacclimation to fluctuating irradiance in an Antarctic diatom and a green flagellate. Mar Ecol Prog. 2005;288(1):9–19.

    Google Scholar 

  23. 23.

    Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV. Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol. 2010;12(1):95–104.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Croteau D, Guérin S, Bruyant F, Ferland J, Campbell DA, Babin M, Lavaud J. Contrasting nonphotochemical quenching patterns under high light and darkness aligns with light niche occupancy in Arctic diatoms. Limnol Oceanogr. 2021;66(S1).

  25. 25.

    Smayda TJ. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanogr. 1997;42(5part2):1137–53.

    Google Scholar 

  26. 26.

    Berdalet E, Peters F, Koumandou VL, Roldan C, Guadayol O, Estrada M. Species-specific physiological response of dinoflagellates to quantified small-scale turbulence 1. J Phycol. 2007;43(5):965–77.

    Google Scholar 

  27. 27.

    Margalef R. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol Acta. 1978;1(4):493–509.

    Google Scholar 

  28. 28.

    Zielinski BL. Eukaryotic gene expression patterns of microorganisms in the Amazon River plume parallel the biogeochemistry of plume waters. Dissertations Theses-Gradworks. 2014.

  29. 29.

    Capone DG, Hutchins DA. Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nat Geosci. 2013;6(9):711–7.

    CAS  Google Scholar 

  30. 30.

    Shin KH, Hama T, Yoshie N, Noriki S, Tsunogai S. Dynamics of fatty acids in newly biosynthesized phytoplankton cells and seston during a spring bloom off the west coast of Hokkaido Island, Japan. Mar Chem. 2000;70(4):243–56.

    CAS  Google Scholar 

  31. 31.

    Olesen M. Comparison of the sedimentation of a diatom spring bloom and of a subsurface chlorophyll maximum. Mar Biol. 1995;121(3):541–7.

    Google Scholar 

  32. 32.

    Levandowsky M, Kaneta PJ. Behaviour in dinoflagellates. Biol Dinoflagellates. 1987:360–97.

  33. 33.

    Lim AS, Jeong HJ, Ok JH, You JH, Kang HC, Kim SJ. Effects of light intensity and temperature on growth and ingestion rates of the mixotrophic dinoflagellate Alexandrium pohangense. Mar Biol. 2019;166(7):98.

    Google Scholar 

  34. 34.

    Long SP, S Humphries A, Falkowski PG. Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol. 1994;45(1):633–62.

    CAS  Google Scholar 

  35. 35.

    Keating K: Seasonal variation of diatoms and dinoflagellates in Monterey Bay, CA determined by Chemtax alanysis of HPLC pigment data. California Sea Grant College Program 2013.

  36. 36.

    Kudela RM, Cochlan WP, Dugdale RC. Carbon and nitrogen uptake response to light by phytoplankton during an upwelling event. J Plankton Res. 1997;19(5):609–30.

    Google Scholar 

  37. 37.

    Buck KR, Uttalcooke L, Pilskaln CH, Roelke DL, Villac MC, Fryxell GA, Cifuentes L, Chavez FP. Autecology of the diatom Pseudonitzschia-Australis, a Domoic acid producer, from Monterey Bay, California. Mar Ecol Prog Ser. 1992;84(3):293–302.

    Google Scholar 

  38. 38.

    Chavez FP. Forcing and biological impact of onset of the 1992 El Nino in Central California. Geophys Res Lett. 1996;23(3):265–8.

    Google Scholar 

  39. 39.

    Abrantes F. Diatom assemblages as upwelling indicators in surface sediments off Portugal. Mar Geol. 1988;85(1):15–39.

    Google Scholar 

  40. 40.

    Margalef R. Phytoplankton communities in upwelling areas. The example of NW Africa. Oecologia aquatica. 1978:3(3).

  41. 41.

    Lampe RH, Cohen NR, Ellis KA, Bruland KW, Maldonado MT, Peterson TD, Till CP, Brzezinski MA, Bargu S, Thamatrakoln K. Divergent gene expression among phytoplankton taxa in response to upwelling. Environ Microbiol. 2018;20(8):3069–82.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Barber R, Smith R: Coastal upwelling ecosystems in Longhurst, AR, ed., Analysis of Marine Ecosystems. In.: London, Academic Press; 1981.

  43. 43.

    Wilkerson F, Dugdale R, Kudela R, Chavez F. Biomass and productivity in Monterey Bay, California: contribution of the large phytoplankton. Deep-Sea Res II Top Stud Oceanogr. 2000;47(5–6):1003–22.

    Google Scholar 

  44. 44.

    Hood RR, Abbott MR, Huyer A, Kosro PM. Surface patterns in temperature, flow, phytoplankton biomass, and species composition in the coastal transition zone off northern California. J Geophys Res Oceans. 1990;95(C10):18081–94.

    Google Scholar 

  45. 45.

    Álvarez-Salgado XA, Nieto-Cid M, Piedracoba S, Crespo BG, Gago J, Brea S. Origin and fate of a bloom of Skeletonema costatum during a winter upwelling/downwelling sequence in the Ría de Vigo (NW Spain). J Mar Res. 2005;63(6):1127–49.

  46. 46.

    Alvarez-Salgado XA, Rosón G, Pérez FF, Pazos Y. Hydrographic variability off the Rías Baixas (NW Spain) during the upwelling season. J Geophys Res. 1993;98(C8):14447–55.

    Google Scholar 

  47. 47.

    Blanton JO, Tenore KR, Castillejo F, Atkinson LP, Schwing FB, Lavin A. The relationship of upwelling to mussel production in the rias on the western coast of Spain. J Mar Res. 1987;45(2):497–511.

    CAS  Google Scholar 

  48. 48.

    Pitcher G, Boyd A. Across-shelf and alongshore dinoflagellate distributions and the mechanisms of red tide formation within the southern Benguela upwelling system. Harmful Toxic Algal Blooms. 1996:243–6.

  49. 49.

    Figueiras F, Pitcher G, Estrada M. Harmful algal bloom dynamics in relation to physical processes. In: Ecology of harmful algae. Springer; 2006. p. 127–138.

  50. 50.

    Smayda T, Trainer VL. Dinoflagellate blooms in upwelling systems: seeding, variability, and contrasts with diatom bloom behaviour. Prog Oceanogr. 2010;85(1–2):92–107.

    Google Scholar 

  51. 51.

    Bailleul B, Berne N, Murik O, Petroutsos D, Prihoda J, Tanaka A, Villanova V, Bligny R, Flori S, Falconet D et al: Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms. Nature 2015, 524(7565):366−+.

  52. 52.

    Finazzi G, Moreau H, Bowler C. Genomic insights into photosynthesis in eukaryotic phytoplankton. Trends Plant Sci. 2010;15(10):565–72.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Kuczynska P, Jemiola-Rzeminska M, Strzalka K. Photosynthetic pigments in diatoms. Mar Drugs. 2015;13(9):5847–81.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Wang W, Yu LJ, Xu C, Tomizaki T, Zhao S, Umena Y, Chen X, Qin X, Xin Y, Suga M, et al. Structural basis for blue-green light harvesting and energy dissipation in diatoms. Science. 2019:363(6427).

  55. 55.

    Grouneva I, Muth-Pawlak D, Battchikova N, Aro EM. Changes in relative thylakoid protein abundance induced by fluctuating light in the diatom Thalassiosira pseudonana. J Proteome Res. 2016;15(5):1649–58.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Jokel M, Johnson X, Peltier G, Aro EM, Allahverdiyeva Y. Hunting the main player enabling Chlamydomonas reinhardtii growth under fluctuating light. Plant J. 2018;94(5):822–35.

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Suorsa M, Jarvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjarvi S, Paakkarinen V, Tikkanen M, Jansson S, et al. PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell. 2012;24(7):2934–48.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Yamori W, Makino A, Shikanai T. A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep-Uk. 2016;6.

  59. 59.

    Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature. 2008;456(7219):239–44.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Depauw FA, Rogato A, d'Alcala MR, Falciatore A. Exploring the molecular basis of responses to light in marine diatoms. J Exp Bot. 2012;63(4):1575–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE. Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol. 2000;36(2):379–86.

    CAS  Google Scholar 

  62. 62.

    Dore JE, Letelier RM, Church MJ, Lukas R, Karl DM. Summer phytoplankton blooms in the oligotrophic North Pacific subtropical gyre: historical perspective and recent observations. Prog Oceanogr. 2008;76(1):2–38.

    Google Scholar 

  63. 63.

    Cui YD, Zhang H, Lin SJ. Enhancement of non-photochemical quenching as an adaptive strategy under phosphorus deprivation in the Dinoflagellate Karlodinium veneficum. Front Microbiol. 2017;8.

  64. 64.

    Zhou Z-X, Yu R-C, Zhou M-J. Seasonal succession of microalgal blooms from diatoms to dinoflagellates in the East China Sea: a numerical simulation study. Ecol Model. 2017;360:150–62.

    Google Scholar 

  65. 65.

    Zhou Y, Zhang Y, Li F, Tan L, Wang J: Nutrients structure changes impact the competition and succession between diatom and dinoflagellate in the East China Sea. Ence of the Total Environment 2017, 574(JAN.1):499–508.

  66. 66.

    Zhou Z-X, Yu R-C, Sun C, Feng M, Zhou M-J. Impacts of Changjiang River discharge and Kuroshio intrusion on the diatom and Dinoflagellate blooms in the East China Sea. J Geophys Res. 2019;124(7):5244–57.

    Google Scholar 

  67. 67.

    Warns A, Hense I, Kremp A. Modelling the life cycle of dinoflagellates: a case study with Biecheleria baltica. J Plankton Res. 2013;35(2):379–92.

    Google Scholar 

  68. 68.

    Klais R, Tamminen T, Kremp A, Spilling K, An BW, Hajdu S, Olli K. Spring phytoplankton communities shaped by interannual weather variability and dispersal limitation: mechanisms of climate change effects on key coastal primary producers. Limnol Oceanogr. 2013;58(2):753–62.

    Google Scholar 

  69. 69.

    Carreto JI, Carignan MO, Montoya NG, Cozzolino E, Akselman R. Mycosporine-like amino acids and xanthophyll-cycle pigments favour a massive spring bloom development of the dinoflagellate Prorocentrum minimum in Grande Bay (Argentina), an ozone hole affected area. J Marine Syst. 2018;178:15–28.

    Google Scholar 

  70. 70.

    Spilling K, Markager S. Ecophysiological growth characteristics and modeling of the onset of the spring bloom in the Baltic Sea. J Marine Syst. 2008;73(3–4):323–37.

    Google Scholar 

  71. 71.

    van de Poll WH, Abdullah E, Visser RJW, Fischer P, Buma AGJ. Taxon-specific dark survival of diatoms and flagellates affects Arctic phytoplankton composition during the polar night and early spring. Limnol Oceanogr. 2020;65(5):903–14.

    Google Scholar 

  72. 72.

    Kamp A, de Beer D, Nitsch JL, Lavik G, Stief P. Diatoms respire nitrate to survive dark and anoxic conditions. P Natl Acad Sci USA. 2011;108(14):5649–54.

    CAS  Google Scholar 

  73. 73.

    Lacour T, Morin P-I, Sciandra T, Donaher N, Campbell D, Ferland J, Babin M. Decoupling light harvesting, electron transport and carbon fixation during prolonged darkness supports rapid recovery upon re-illumination in the Arctic diatom Chaetoceros neogracilis. Polar Biol. 2019.

  74. 74.

    Hauss H, Franz JMS, Sommer U. Changes in N:P stoichiometry influence taxonomic composition and nutritional quality of phytoplankton in the Peruvian upwelling. J Sea Res. 2012;73:74–85.

    CAS  Google Scholar 

  75. 75.

    Falkowski PG, Barber RT, Smetacek VV. Biogeochemical controls and feedbacks on ocean primary production. Science. 1998;281(5374):200–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Tian Y, Mingjiang Z, Peiyuan Q. Competition among DinoflagellateAlexandrium tamarense, raphidophyteHeterosigma carterae and diatomSkeletonema costatum under combinations of two temperatures and five salinities. Chin J Oceanol Limnol. 2003;21(3):245–50.

    Google Scholar 

  77. 77.

    Kiørboe T, Tiselius P, Mitchell-Innes B, Hansen JL, Visser AW, Mari X. Intensive aggregate formation with low vertical flux during an upwelling-induced diatom bloom. Limnol Oceanogr. 1998;43(1):104–16.

    Google Scholar 

  78. 78.

    Raven J: The vacuole: a cost-benefit analysis. In: Advances in Botanical Research. vol. 25: Elsevier; 1997: 59–86.

  79. 79.

    Wang J, Zhang Y, Li H, Cao J. Competitive interaction between diatom Skeletonema costatum and dinoflagellate Prorocentrum donghaiense in laboratory culture. J Plankton Res. 2012;35(2):367–78.

    Google Scholar 

  80. 80.

    Burkholder JM, Glibert PM, Skelton HM. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae. 2008;8(1):77–93.

    CAS  Google Scholar 

  81. 81.

    Stoecker D, Tillmann U, Granéli E: Phagotrophy in Harmful Algae. In: Ecology of Harmful Algae. Edited by Granéli E, Turner JT. Berlin, Heidelberg: Springer Berlin Heidelberg; 2006: 177–187.

  82. 82.

    Fenchel TOM. How Dinoflagellates swim. Protist. 2001;152(4):329–38.

    CAS  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Eppley RW, Holm-Harisen O, Strickland JDH: SOME OBSERVATIONS ON THE VERTICAL MIGRATION OFDINOFLAGELLATES. 1968.

  84. 84.

    Cullen JJ, Horrigan SG. Effects of nitrate on the diurnal vertical migration, carbon to nitrogen ratio, and the photosynthetic capacity of the dinoflagellate Gymnodinium splendens. Mar Biol. 1981;62(2):81–9.

    CAS  Google Scholar 

  85. 85.

    Domingues RB, Anselmo TP, Barbosa AB, Sommer U, Galvao HM. Light as a driver of phytoplankton growth and production in the freshwater tidal zone of a turbid estuary. Estuar Coast Shelf S. 2011;91(4):526–35.

    CAS  Google Scholar 

  86. 86.

    Furnas M. In situ growth rates of marine phytoplankton: approaches to measurement, community and species growth rates. J Plankton Res. 1990;12:1117–51.

    Google Scholar 

  87. 87.

    K K, Seike Y, Date Y. Red tides in the brackish Lake Nakanoumi (III). The stimulative effects of organic substances in the interstitial water of bottom sediments and in the excreta from Skeletonema costatum on the growth of Prorocentrum minimum. Bulletin Plankton Soc Japan. 1990;37:p35–47.

    Google Scholar 

  88. 88.

    Heydarizadeh P, Veidl B, Huang B, Lukomska E, Wielgosz-Collin G, Couzinet-Mossion A, Bougaran G, Marchand J, Schoefs B. Carbon Orientation in the Diatom Phaeodactylum tricornutum: The Effects of Carbon Limitation and Photon Flux Density. Front Plant Sci. 2019:10(471).

  89. 89.

    Anning T, MacIntyre HL, Pratt SM, Sammes PJ, Gibb S, Geider RJ. Photoacclimation in the marine diatom Skeletonema costatum. Limnol Oceanogr. 2000;45(8):1807–17.

    Google Scholar 

  90. 90.

    Janknegt P, van de Poll W, Visser R, Rijstenbil J, Buma A. Oxidative stress responses in the marine Antarctic diatom Chaetoceros brevis (Bacillariophyceae) during photoacclimation. J Phycol. 2008;44:957–66.

    CAS  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Cartaxana P, Cruz S, Gameiro C, Kühl M. Regulation of Intertidal Microphytobenthos Photosynthesis Over a Diel Emersion Period Is Strongly Affected by Diatom Migration Patterns. Front Microbiol. 2016:7(872).

  92. 92.

    Hong-Bo T. Study on the DINOFLAGELLATE bloom in the three gorges reservoir and the DONGHU Lake, WUHAN. 2006.

  93. 93.

    Klinger CM, Paoli L, Newby RJ, Wang MYW, Carroll HD, Leblond JD, Howe CJ, Dacks JB, Bowler C, Cahoon AB, et al. Plastid transcript editing across Dinoflagellate lineages shows lineage-specific application but conserved trends. Genome Biol Evol. 2018;10(4):1019–38.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. 94.

    Evens TJ, Kirkpatrick GJ, Millie DF, Chapman DJ, Schofield OME. Photophysiological responses of the toxic red-tide dinoflagellate Gymnodinium breve (Dinophyceae) under natural sunlight. J Plankton Res. 2001;23(11):1177–94.

    CAS  Google Scholar 

  95. 95.

    Shi XG, Li L, Guo CT, Lin X, Li MZ, Lin SJ. Rhodopsin gene expression regulated by the light dark cycle, light spectrum and light intensity in the dinoflagellate Prorocentrum. Front Microbiol. 2015;6.

  96. 96.

    Kono M, Terashima I. Elucidation of Photoprotective mechanisms of PSI against fluctuating light photoinhibition. Plant Cell Physiol. 2016;57(7):1405–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  97. 97.

    Leister D, Shikanai T. Complexities and protein complexes in the antimycin A-sensitive pathway of cyclic electron flow in plants. Front Plant Sci. 2013;4:161.

    PubMed  PubMed Central  Google Scholar 

  98. 98.

    Storti M, Alboresi A, Gerotto C, Aro E-M, Finazzi G, Morosinotto T. Role of cyclic and pseudo-cyclic electron transport in response to dynamic light changes in Physcomitrella patens. Plant Cell Environ. 2018;0(0).

  99. 99.

    Guillard RR, Ryther JH. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) gran. Can J Microbiol. 1962;8:229–39.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. 100.

    Lavaud J, Strzepek RF, Kroth PG. Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnol Oceanogr. 2007;52(3):1188–94.

    CAS  Google Scholar 

  101. 101.

    Allahverdiyeva Y, Mustila H, Ermakova M, Bersanini L, Richaud P, Ajlani G, Battchikova N, Cournac L, Aro EM. Flavodiiron proteins Flv1 and Flv3 enable cyanobacterial growth and photosynthesis under fluctuating light. P Natl Acad Sci USA. 2013;110(10):4111–6.

    CAS  Google Scholar 

  102. 102.

    Zhou L, Gao S, Wu S, Han D, Wang H, Gu W, Hu Q, Wang J, Wang G. PGRL1 overexpression in Phaeodactylum tricornutum inhibits growth and reduces apparent PSII activity. Plant J. 2020;103(5):1850–7.

  103. 103.

    Hehenberger E, Gast RJ, Keeling PJ. A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis. P Natl Acad Sci USA. 2019;116(36):17934–42.

    CAS  Google Scholar 

  104. 104.

    Yuzao Q, Chanjiang H, Yan Z, Lei Z. Laboratory study on the diurnal vertical migration of a poisonous red-tide DINOFLAGELLATE ALEXANDRIUM TAMARENSE. Oceanologia Et Limnologia Sinica. 1997;05:458–67.

    Google Scholar 

  105. 105.

    Wu SC, Huang AY, Zhang BY, Huan L, Zhao PP, Lin AP, Wang GC. Enzyme activity highlights the importance of the oxidative pentose phosphate pathway in lipid accumulation and growth of Phaeodactylum tricornutum under CO2 concentration. Biotechnol Biofuels. 2015;8.

  106. 106.

    Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, Mcginnis S, Madden TL. NCBI Blast: a better web interface. 2008.

  107. 107.

    Ladner JT, Barshis DJ, Palumbi SR. Protein evolution in two co-occurring types of Symbiodinium: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evol Biol. 2012;12(1):217.

  108. 108.

    Shoguchi E, Shinzato C, Kawashima T, Gyoja F, Mungpakdee S, Koyanagi R, Takeuchi T, Hisata K, Tanaka M, Fujiwara M, Hamada M, Seidi A, Fujie M, Usami T, Goto H, Yamasaki S, Arakaki N, Suzuki Y, Sugano S, Toyoda A, Kuroki Y, Fujiyama A, Medina M, Coffroth MA, Bhattacharya D, Satoh N. Draft Assembly of the symbiodinium minutum nuclear genome reveals dinoflagellate gene structure. Curr Biol. 2013;23(15):1399–408.

  109. 109.

    Lin S, Cheng S, Song B, Zhong X, Lin X, Li W, Li L, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y, Shi X, Lin L, Wang L, Wang Z, Liu X, Yu S, Zeng P, Hao H, Zou Q, Chen C, Li Y, Wang Y, Xu C, Meng S, Xu X, Wang J, Yang H, Campbell DA, Sturm NR, Dagenais-Bellefeuille S, Morse D. The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science. 2015;350(6261):691–4.

  110. 110.

    Rosic N, Ling EWS, Chan C-KK, Lee HC, Kaniewska P, Edwards D, Dove S, Hoegh-Guldberg O. Unfolding the secrets of coral–algal symbiosis. ISME J. 2015;9(4):844–56.

  111. 111.

    Xiang T, Nelson W, Rodriguez J, Tolleter D, Grossman AR. Plant J. 2015;82(1):67–80.

  112. 112.

    Shi X, Lin X, Li L, Li M, Palenik B, Lin S. Transcriptomic and microRNAomic profiling reveals multi-faceted mechanisms to cope with phosphate stress in a dinoflagellate. ISME J. 2017;11(10):2209–18.

  113. 113.

    Shoguchi E, Beedessee G, Tada I, Hisata K, Kawashima T, Takeuchi T, Arakaki N, Fujie M, Koyanagi R, Roy MC, Kawachi M, Hidaka M, Satoh N, Shinzato C. Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes. BMC Genomics 2018;19(1).

  114. 114.

    Yuyama I, Ishikawa M, Nozawa M, Yoshida M, Ikeo K. Transcriptomic changes with increasing algal symbiont reveal the detailed process underlying establishment of coral-algal symbiosis. Sci Rep. 2018;8(1).

  115. 115.

    Wang X, Niu X, Chen Y, Sun Z, Han A, Lou X, Ge J, Li X, Yang Y, Jian J, Gonçalves RJ, Guan W. Transcriptome sequencing of a toxic dinoflagellate, Karenia mikimotoi subjected to stress from solar ultraviolet radiation. Harmful Algae. 2019;88:101640.

  116. 116.

    Silva Lima AW, Leomil L, Oliveira L, Varasteh T, Thompson JR, Medina M, Thompson CC, Thompson FL. Insights on the genetic repertoire of the coral Mussismilia braziliensis endosymbiont Symbiodinium. Symbiosis. 2020;80(2):183–93.

  117. 117.

    Timothy B, Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. 1994.

  118. 118.

    Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE. Transformation of the diatom Phaeodactylum Tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol. 2010;36(2):379–86.

    Google Scholar 

  119. 119.

    Apt KE, Grossman AR, Kroth-Pancic PG. Stable nuclear transformation of the diatomPhaeodactylum tricornutum. Mol Gen Genet MGG. 1996;252(5):572–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 120.

    Grouneva I, Rokka A, Aro EM. The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J Proteome Res. 2011;10(12):5338–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  121. 121.

    Zheng ZB, Gao S, Wang GC. Far red light induces the expression of LHCSR to trigger nonphotochemical quenching in the intertidal green macroalgae Ulva prolifera. Algal Res. 2019;40.

  122. 122.

    Ritchie RJ. Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res. 2006;89(1):27–41.

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We appreciate the contribution of Yusuke Matsuda and Chris Bowler for kindly gifting us vectors. We appreciate Toshiharu Shikanai and Yingzhong Tang for useful advice. We also appreciate Zhiming Yu for donating P. donghaiense. We thank Wiley editing services for editing this manuscript (https://wileyeditingservices.com/en/).

Funding

This work was supported by the National Key R&D Program of China (2018YFD0901500), the Key Deployment Project of the Centre for Ocean Mega-Research of Science, the Chinese Academy of Sciences (COMS2019Q02), the Shandong Provincial R&D Program (2018GHY115019), the Distinguished Young Scientists Research Fund of the Key Laboratory of Experimental Marine Biology, the Chinese Academy of Sciences (No. KLEMB-DYS02), and the National Natural Science Foundation of China (41676157 and 41976097).

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G.W. and S.G. conceived the research, and L.Z. designed the work. L.Z., S.G., S.W., W.G., L.W. and J.W. conducted the experiments and analyzed the data. L.Z. S.G. and G.W. drafted modified the manuscript and all authors approved. All authors read and approved the final manuscript.

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Correspondence to Shan Gao or Guangce Wang.

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The original online version of this article was revised: the authors identified that Figure 3 appears identical with Figure 4. In fact, the figure 3 has never been changed from the original submitted manuscript to the revision and proof process. The order and legend of figure 3 were also not changed in the submission and revision. The loss of figure 3 was due to the careless manipulation during the typesetting process.

Supplementary Information

Additional file 1: Figure S1.

Y(NA) (PSI acceptor side limitation), Y(ND) (PSI donor side limitation), and 1–qL (PQ redox state) of red tide diatom S. costatum, red tide dinoflagellate A. carterae, P. donghaiense, and K. mikimotoi, model diatom P. tricornutum, T. pseudonana and model dinoflagellate D. Symbiodinium under (A) mild light fluctuation after the addition of 1 min of bright light (800 μmol photons m-2 s-1) to every 5 min of low light (80 μmol photons m-2 s-1) and (B) severe light fluctuation after the addition of 1 min of stronger light (2,000 μmol photons m-2 s-1) to every 5 min of low light (20 μmol photons m-2 s-1).

Additional file 2: Figure S2.

Conserved sequences in, and evolutionary relationships of, PGR5 in plants and algae. Known signal peptide sequences are underlined. Motifs were identified using the MEME motif elicitation tool (Version 5.0.5). The missing conserved sites of dinoflagellates are shown with a red cross. The sequences are available in NCBI database (http://www.ncbi.nlm.nih.gov) or UniProtKB/TrEMBL database (https://www.uniprot.org/) as following. Eudicots: Arabidopsis thaliana (gi: 330250863), Cucumis sativus (gi: 164449273), Artemisia annua (gi: 1387830212), Gossypium arboreum (tr: I1ZIR9); Amborella: Amborella trichopoda (gi: 586688763); Gymnosperm: Pinus taeda (gi: 196168724); monocots: Triticum aestivum (gi: 393690734), Brachypodium distachyon (gi: 357144276), Oryza brachyantha (gi: 573956334), Panicum hallii (gi: 1435170242), Zea mays (gi: 1394909989); Mosses: Physcomitrella patens (gi: 1373914553); Klebsormidiales: Klebsormidium nitens (gi: 971519293); Chlorophyta: Tetrabaena socialis (gi: 1331346858), Monoraphidium neglectum (gi: 926775414), Auxenochlorella protothecoides (gi: 675355490); Cyanobacteria: Acaryochloris marina MBIC11017 (gi: 158308814), Cyanothece sp. PCC 7425 (gi: 219867356); Rhodophyta: Porphyra umbilicalis (gi: 1189386569), Pyropia yezoensis (tr: A1YSQ5), Gracilariopsis chorda (gi: 1395913517), Phaeophyta: Ectocarpus siliculosus (tr: D7G229); Diatom: Thalassiosira pseudonana (tr: B8C035), Phaeodactylum tricornutum (strain CCAP 1055/1) (tr: B7FVH9); Dinoflagellates: sequences were identified using NCBI-BLAST (BASF01, BGNK01, BGPT01, GAFO01, GBSC01, GFLM01, GFPM01, GHKS01, GICE01, IADN01, IADM01, VSDK0, PRJNA374496).

Additional file 3: Figure S3.

Relative (A) RNA levels of PGR5 under 80 μmol photons m-2 s-1 and (B) thylakoid membrane protein levels (PGR5, PsaB, and AtpB) in the WT, 5OE-1, and 5KN-i1 under different light conditions. The protein was quantified using the BCA method (50 μg protein, ~3 μg Chl). CL: constant light under 80 μmol photons m-2 s-1; mFL: mildly fluctuating light: addition of 1 min of bright light (800 μmol photons m-2 s-1) to every 5 min of low light (80 μmol photons m-2 s-1); sFL: severely fluctuating light: addition of 1 min of stronger light (2,000 μmol photons m-2 s-1) to every 5 min of low light (20 μmol photons m-2 s-1). ANOVA was calculated by SPSS 23.0 (P<0.01).

Additional file 4: Table S1.

. Primers used in transgene construction. The restriction sites are shown in bold.

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Zhou, L., Wu, S., Gu, W. et al. Photosynthesis acclimation under severely fluctuating light conditions allows faster growth of diatoms compared with dinoflagellates. BMC Plant Biol 21, 164 (2021). https://doi.org/10.1186/s12870-021-02902-0

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Keywords

  • Diatoms
  • Dinoflagellates
  • Fluctuating light
  • Pioneer bloom
  • PGR5
  • Phaeodactylum tricornutum
  • Phytoplankton bloom succession