Picophytoplankton have a competitive advantage for nutrient uptake in oligotrophic environments where they contribute significantly to the total Chl a 1–3. However, several observations have pointed out the ecological relevance of picophytoplankton also in coastal and eutrophic environments 9,11,13,50. Information about the seasonal abundance of picophytoplankton in the Baltic Sea is limited. As a consequence, picophytoplankton biomass contribution is frequently estimated using Chl a fractionation 14–18 or not included in the calculations 51,52. At the K-station during 2018, Synechococcus was present throughout the year, with maximum abundances during summer (4.7 x 105 cells mL− 1). These numbers were comparable to other observations in the Baltic Sea Proper during summer 32,39, suggesting that Synechococcus abundances at the coast are as high as in offshore locations. PPE abundances reached 1.1 x 105 cells mL− 1 during spring, around two orders of magnitude higher than the maximum abundances reported from the Gulf of Finland 26 and one order of magnitude higher than the maximum observed in other estuaries 29,53. The current study (K-station) highlights the significant contribution of Synechococcus and PPE to the total phytoplankton biomass in the estuarine and eutrophic coastal Baltic Sea over an annual cycle.
Picophytoplankton is composed of multiple functional groups spanning diverse physiological adaptations and niches 17,29. Recent studies, in other estuarine and coastal areas, have separated Synechococcus into pigment based functional groups (PE-rich and PC-rich) suggesting significant differences in distribution patterns between the groups 13,54,55. In this study, the three functional groups, PE-rich, PC-rich and PPE and had significant differences in regard to, 1) seasonal dynamics, 2) biomass contribution, 3) temperature regimes, and 4) nutrient limitation. These results emphasize the importance of high-resolution studies of ecological relevant functional groups in order to understand the dynamics of the genetic and physiologically diverse picophytoplankton 21,56.
Seasonal variations in the PE-rich and PC-rich contributions to the Synechococcus community has previously been observed in tropical and subtropical estuaries 28,29,34,55. At the K-station, PE-rich and PC-rich abundance increased during spring and peaked during early summer while this period PE-rich dominated the Synechococcus community. This was consistent with previous observations of PE-rich dominance in the Baltic Sea during the spring-summer period 17,31,32. During the autumn, PE-rich abundance declined resulting in PC-rich dominance. These novel findings are in line with different temperature adaptations between PE-rich and PC-rich groups 29. These field observations also support the experimental evidence that PC-rich isolates are better adapted to lower irradiance than PE-rich 57. PPE increase in abundance is usually related to low temperatures and high nutrient concentration 26,36. Our observations showed that PPE abundances peaked during spring, at 11–15°C. The low PPE abundance during autumn contrast with the peak abundances observed by Kuosa et al.26 during the same period. These patterns could be explained by the long lasting summer of 2018 58 which could have shifted PPE favorable temperatures to later in the autumn while concurrent light limitation may have restricted PPE growth 37.
The biomass estimates at the K-station, confirmed that the pico-fraction is a major contributor to the total phytoplankton biomass 17,18,59 and can dominate the phytoplankton community during spring, early summer and autumn. Resolving the biomass estimates into the three functional groups reveal that on an annual basis, PPE was the main contributor except during the bloom of N2-fixing cyanobacteria at the end of July (> 18°C). This highlights the importance of PPE in coastal environments 60. High contribution of both Synechococcus groups concur with high temperatures, in line with previous studies 15. A community composition shift from PPE to Synechococcus can have a large impact for the microbial food web and should be systematically included in future phytoplankton biomass studies and carbon flux models 61.
Niche adaptation to temperature show different patterns among the picophytoplankton groups. Bioassays at the K-station showed the highest net growth rates during spring and beginning of the summer at 10°C and 17–19°C for PE-rich and 11–15°C for PPE. The temperature niche for PC-rich was 13–16°C leading to the highest net growth rates during autumn. The net growth rates of Synechococcus were in line with previous observations in temperate ecosystems (Table 2). Similarly to the high-resolution growth dynamic study by Hunter-Cevera et al.62, in this Baltic Sea study, net growth showed no increase at > 16–17°C. However, higher net growth rates of Synechococcus (up to 2.86 d− 1) have been reported in warmer climate (Table 2). Thus, an increase in temperature due to climate change might result in an increase of Synechococcus growth at higher latitudes 63. The calculated net growth rates in the bioassays did not follow the same seasonality as the in situ net growth rates due to the high weekly variation in picophytoplankton cell abundance. These results underscore the importance of high resolution sampling when studying picophytoplankton dynamics.
The bioassays showed that NH4 was the preferred form of nitrogen for picophytoplankton. The preference of NH4 over NO3 for Synechococcus has been extensively documented 42–44, 46,47. This study shows that both PE-rich and PC-rich can use NO3 and NH4 at low temperature but prefer NH4 at high temperature (> 15–17°C). This is in line with the effect of temperature on nitrogen assimilation enzymatic pathways 41. The assimilation of NH4 generally occurs through the GS-GOGAT pathway, while NO3 uptake depends on the enzyme nitrate reductase (NR). GS-GOGAT is positively correlated with temperature meanwhile NR is negatively correlated 41. As a result, NH4 assimilation will be higher than NO3 assimilation at high temperatures. Thus, the uptake of NH4 is an advantageous adaptation for Synechococcus to compete with other NO3 specialists such as diatoms under nitrogen limitation during the warm periods 41. It should be noted, that our results shows that PE-rich is better adapted to high temperatures than PC-rich, and as a consequence PE-rich may benefit more from NH4 uptake. In coastal areas and shallow water ecosystems (< 50 m depth) NH4 from benthic or riverine origin can be the main nitrogen source for the phytoplankton community 46,64, which could benefit PE-rich at high temperatures. The correlation between PE-rich and N2-fixing cyanobacteria supports that newly fixed nitrogen in the form of NH4 may have a key role in controlling PE-rich abundance 14,38,48. In line with the observations by Berthelot et al.47, PPE growth increased in NH4 addition treatments during nitrogen limitation. However, nutrient additions at suboptimal temperatures (outside of the temperature niche) resulted in significant reductions of the net growth rates of PPE. This was likely because nutrient addition in a nutrient limited system can favor competitors better adapted for high temperatures such as PE-rich.
This study provides the first annual high resolution description of picophytoplankton abundance and dynamics in the coastal Baltic Sea. It also investigates net growth rates and nutrient limitation of three functional picophytoplankton groups. In this study, PE-rich, PC-rich and PPE showed different seasonal dynamics defined by different temperature niches and nutrient limitation. PPE dynamics in the Baltic Sea are severely understudied. This study shows, for the first time, the importance of picophytoplankton over a full annual cycle and situates PPE as one of the most important components of the phytoplankton community in terms of biomass especially during spring and early summer. The results further suggest that in eutrophic coastal systems where NH4 is the main nitrogen-species (agricultural landscape), PE-rich will be favored over PPE. This effect could be further magnified during earlier and more extensive blooms of N2-fixing cyanobacteria that are projected as a consequence of global warming 65,66. Such events could favor PE-rich over PC-rich and PPE, leading to picophytoplankton community shifts having profound consequences on the contribution to the total carbon biomass in coastal areas.