Silicon Accumulation By Picophytoplankton In Oligotrophic Oceans

Picophytoplankton play a key role in initiating and supporting food web and energy flow in the ocean,and also are major contributors to the global marine carbon(C)cycle.In recent years,they have been found to have significant silica(Si)accumulation,a finding which provides a new sight into the interaction of marine Si and C cycles and questions the overwhelming role of diatoms in oceanic Si-C cycles.In the face of such high cell abundance,genetic diversity and wide distribution of picophytoplankton in the open ocean,exploring their influences on oceanic Si-C cycles and other element cycles as well as their responses to global climate change are becoming new scientific hotspots,and relevant research needs to be carried out urgently.However,there are still few studies on the physiology and ecology of picophytoplankton in oligotrophic oceans,especially their roles in the marine Si-C cycles and other element cycles,relevant data are very scarce.Therefore,it is necessary to accurately quantify the contributions of picophytoplankton to the oceanic Si-C cycles,and clarify their Si-C sinking mechanisms,and explore their significance in marine Si-C interaction.As the Eastern Indian Ocean(EIO)and Western Pacific Ocean(WPO)belong to extremely oligotrophic gryes,where the global oceanographic studies have not been paid much attention on biology,there are few studies on the contributions of picophytoplankton to Si-C cycles in the oligotrophic EIO and WPO.In the present study,we expect to have a systematic and comprehensive understanding of picophytoplankton Si-C accumulation and regulation mechanism in the oligotrophic EIO and WPO,and even in the global ocean by conducting targeted studies on these scientific issues.This also provides a premise foundation and theoretical framework for further study of the role of picophytoplankton in the global ocean Si cycle and the coupling of Si-C cycles.Marine picophytoplankton are abundant in many oligotrophic oceans,but the known geographical patterns of picophytoplankton are primarily based on small-scale cruises or time-series observations.Here we conducted a wider oceanographic survey(5 cruises)in the Bay of Bengal(BOB),South China Sea(SCS)and Western Pacific Ocean(WPO)to better understand the biogeographic variations of marine picophytoplankton.Prochlorococcus were the most abundant picophytoplankton(averaging 1.9-3.6×104 cells ml-1)across the three seas,while average abundances of Synechococcus and picoeukaryotes were generally 1-2 orders of magnitude lower than Prochlorococcus.Average abundances of total picophytoplankton were similar between the BOB and SCS(4.7×104 cells ml-1),but were 2-3 folds less abundant in the WPO(2.5×104 cells ml-1).Synechococcus and Prochlorococcus accounted for a substantial fraction of total picophytoplankton carbon(C)biomass(70-83%)in the three contrasting seas,indicating the ecological importance of Synechococcus and Prochlorococcus as primary producers.Prochlorococcus were generally abundant in the oligotrophic open waters,however,the exceptional presence of Prochlorococcus near the SCS coast was potentially associated with the Kuroshio intrusion.Synechococcus and picoeukaryotes abundances were higher near the fresh water-dominated areas,which was likely due to the dilution waters.Water temperature and cold eddy were also major drivers responsible for the biogeographic distributions of picophytoplankton.Although Synechococcus,Prochlorococcus and picoeukaryotes showed negative correlations with nutrient concentrations,the maximal abundances of them in vertical distribution showed positive correlations with the nutricline depth,indicating the nutrient availability has two-faceted role in regulating the biogeographic variations of picophytoplankton.Dynamics of picophytoplankton and photosynthesis will be inevitably impacted by changing marine environment,such as ocean acidification and nutrient supply,but related studies are very scarce.Here we cultured the picophytoplankton-dominated surface water of the oligotrophic EIO at two le-vels of pCO2(400 and 1000 ppm)and phosphate(0.05 and 1.50 ?M)to investigate the interactive effects of elevated pCO2 and phosphate(P)on the dynamics of picophytoplankton and photosynthetic properties.High pCO2 and P levels interactively increased the abundances of Synechococcus,Prochlorococcus and picoeukaryotes by 33%,18%,and 21%,respectively,of which high P level had a major promoting effect.Conversely,rising pCO2 alone decreased their abundances by 9%,32%,and 46%,respectively.For the photophysiological responses in relation to the combination of high pCO2 and P levels,there was an increase in the maximum(Fv/Fm)and effective(Fq'/Fm')photochemical efficiency,the electron transfer rates(ETRRC?)and the charge separation rates(JVPS?,an indicator of primary production),but a decrease in the non-photochemical quenching(NPQNSV).Elevated pCO2 alone facilitated the NPQNSV process significantly,ultimately leading to reduced light use efficiency(e.g.,Fv,/Fm,Fq'/Fm' and ETRRC?)and primary production(JVPS?).There was a strong coupling of picophytoplankton and JVPS?,suggesting the future EIO primary productivity was potentially controlled by picophytoplankton.Overall,our results indicate that the negative effects caused by ocean acidification may be masked or outweighted by the role that P availability plays in regulating growth and metabolism in this oligotrophic ecosystem.All over the world,the present study involves the first measurements of size-fractionated(i.e.,0.2-2 ?m;2-20 ?m;>20 ?m)biogenic silica(bSi)standing stocks and production rates in the oligotrophic EIO and WPO.In the oligotrophic EIO,the 150 m integrated bSi standing stocks in the pico-and nano-sized fractions averaged 49%and 39%,respectively,of the total;the contributions of pico-and nanophyplankton to total bSi production rates were 43%and 38%,respectively,together suggesting that these smaller phyplankton contributed a significant proportion of both the total bSi standing stock and its rate of production.The total bSi variability appeared to be driven by smaller-phyplankton dynamics.Also,our results suggest that the detrital bSi were potentially sustained by the pico-and nano-sized siliceous organisms(e.g.,Minidiscus and Synechococcus)instead of broken fragments of large diatoms or other siliceous microphyplankton.In particular,the atomically-dense structure from Synechococcus cell lysis was enriched in Si element compared with intact cells.In the complex and varied marine environment,the factors controlling size-fractionated bSi standing stocks may be biological rather than physical processes,and the clear correlation between picoeukaryotes and the<2 ?m bSi further confirmed the possibility of Si accumulation by other smaller phyplankton.In the oligotrophic WPO,based on the size-fractionated bSi analysis,we also observed picophytoplankton contributed a measurable and significant proportion of total bSi standing stocks.The depth-weighted average bSi stock in the<2 ?m size fraction averaged 65%of the total,indicating the magnitude of total bSi standing stocks was driven by the pico-sized fraction in the WPO.While large diatoms had a relevant contribution to the>20 ?m bSi standing stock,this significant contribution of pico-sized fraction to total bSi standing stocks was associated with picocyanobacteria.Interestingly,our estimated contributions of living Synechococcus alone to the<2 ?m bSi standing stock and total bSi standing stocks were small,only averaging 9%and 6%,respectively.Thus we suggested that these small but persistent contributions of living Synechococcus to the bSi standing stocks may be influenced by the detrital bSi or other siliceous organisms(e.g.,Minidiscus comicus).Furthermore,water temperature had a potential effect on the variability of pico-sized fraction bSi stock.Overall,these results provided some new insights into the various environmental and biological factors affecting the oceanic bSi standing stocks.Synechococcus,a small unicellular marine picocyanobacteria that dominate in nutrient-depleted waters,can accumulate substantial amounts Si and are thus thought to exert an influence on the marine Si cycle.To date,however,there are few measurements of Si accumulation in individual Synechococcus cells.To determine the magnitude and variability of Synechococcus cellular Si content in oligotrophic oceans,we analyzed 1348 discrete cells collected from the understudied EIO and WPO.Synechococcus cellular Si quotas varied widely across the EIO and WPO,from 0 to 4651 amol Si cell-1,of which the Si quotas for cells collected from the EIO were between 0 and 2927 amol Si cell-1.While highly variable in range,cells from the WPO had an average of-2.5-fold more Si than cells from the EIO.The estimated contributions of Synechococcus to total and picoplankton bSi stocks were<1-8%and 1-11%,respectively,suggesting that Synechococcus have a small but persistent regional contribution to bSi stocks.These low contributions,however,were quantitatively comparable to that of diatoms in some cases,especially in oligotrophic gyres where diatoms are in low abundance.Additionally,no significant effect of ambient silicic acid concentration on cellular Si quotas was observed within these oligotrophic ecosystems,whereas ambient dissolved inorganic N and P significantly affected Synechococcus cellular Si/S ratio.Similarly,in laboratory culture studies,it was found that silicic acid was not the key control factor for the growth and metabolism of Synechococcus.We suggested that the variance in Si quotas may be indirectly driven by environmental variables via some unknown independent or strain-dependent physiological processes.Finally,combined with our field data above,we have estimated the contributions of picophyplankton and Synechococcus in oligotrophic oceans(e.g.,the EIO and WPO)to the regional and global marine Si-C cycles.Our estimated results showed that global oceanic bSi stocks of picophyplankton were 1.55-3.85 Tmol Si(similar to diatoms),and their C biomass were 0.53-1.32 Pg C.Their global oceanic bSi production were 78-194 Tmol Si yr-1,accounting for 32-80%of total global oceanic bSi production.The Si export flux of picophyplankton were 220 ?mol Si m-2 d-1,contributing 55%of total global oceanic Si export.As such,picophyplankton play an important role in the marine Si cycle at regional and global scales,as well as in the global marine Si-C cycles.In the global ocean,Synechococcus bSi stock was 0.2 Tmol Si,accounting for nearly 5-13%of total picophyplankton bSi stocks and 5-7%of total diatom bSi stocks.Global oceanic bSi production of Synechococcus was 15 Tmol Si yr-1,representing 5-8%of total global oceanic bSi production.Synechococcus Si export was 0.5-3 ?mol Si m-2 d-1,contributing 0.13-0.75%of total global oceanic Si export.Therefore,the contributions of Synechococcus to regional and global bSi stocks/production and export,although small,can not be ignored,and Synechococcus may have a broad geographical impact on the marine Si-C cycles.