Individual and interactive effects of ocean acidification,global warming,and UV radiation on phytoplankton

Rising carbon dioxide (CO₂) concentrations in the atmosphere result in increasing global temperatures and ocean warming (OW). Concomitantly, dissolution of anthropogenic CO₂ declines seawater pH, resulting in ocean acidification (OA) and altering marine chemical environments. The marine biological carbon pump driven by marine photosynthesis plays an important role for oceanic carbon sinks. Therefore, how ocean climate changes affect the amount of carbon fixation by primary producers is closely related to future ocean carbon uptake. OA may upregulate metabolic pathways in phytoplankton, such as upregulating ß-oxidation and the tricarboxylic acid cycle, resulting in increased accumulation of toxic phenolic compounds. Ocean warming decreases global phytoplankton productivity; however, regionally, it may stimulate primary productivity and change phytoplankton community composition, due to different physical and chemical environmental requirements of species. It is still controversial how OA and OW interactively affect marine carbon fixation by photosynthetic organisms. OA impairs the process of calcification in calcifying phytoplankton and aggravate ultraviolet (UV)-induced harms to the cells. Increasing temperatures enhance the activity of cellular repair mechanisms, which mitigates UV-induced damage. The effects of OA, warming, enhanced exposure to UV-B as well as the interactions of these environmental stress factors on phytoplankton productivity and community composition, are discussed in this review.     

The role of phytoplankton photosynthesis in global biogeochemical cycles

Phytoplankton biomass in the world's oceans amounts to only 1–2% of the total global plant carbon, yet these organisms fix between 30 and 50 billion metric tons of carbon annually, which is about 40% of the total. On geological time scales there is profound evidence of the importance of phytoplankton photosynthesis in biogeochemical cycles. It is generally assumed that present phytoplankton productivity is in a quasi steady-state (on the time scale of decades). However, in a global context, the stability of oceanic photosynthetic processes is dependent on the physical circulation of the upper ocean and is therefore strongly influenced by the atmosphere. The net flux of atmospheric radiation is critical to determining the depth of the upper mixed layer and the vertical fluxes of nutrients. These latter two parameters are keys to determining the intensity, and spatial and temporal distributions of phytoplankton blooms. Atmospheric radiation budgets are not in steady-state. Driven largely by anthropogenic activities in the 20th century, increased levels of IR- absorbing gases such as CO₂, CH₄ and CFC's and NO_x will potentially increase atmospheric temperatures on a global scale. The atmospheric radiation budget can affect phytoplankton photosynthesis directly and indirectly. Increased temperature differences between the continents and oceans have been implicated in higher wind stresses at the ocean margins. Increased wind speeds can lead to higher nutrient fluxes. Throughout most of the central oceans, nitrate concentrations are sub-micromolar and there is strong evidence that the quantum efficiency of Photosystem II is impaired by nutrient stress. Higher nutrient fluxes would lead to both an increase in phytoplankton biomass and higher biomass-specific rates of carbon fixation. However, in the center of the ocean gyres, increased radiative heating could reduce the vertical flux of nutrients to the euphotic zone, and hence lead to a reduction in phytoplankton carbon fixation. Increased desertification in terrestrial ecosystems can lead to increased aeolean loadings of essential micronutrients, such as iron. An increased flux of aeolean micronutrients could fertilize nutrient-replete areas of the open ocean with limiting trace elements, thereby stimulating photosynthetic rates. The factors which limit phytoplankton biomass and photosynthesis are discussed and examined with regard to potential changes in the Earth climate system which can lead the oceans away from steady-state. While it is difficult to confidently deduce changes in either phytoplankton biomass or photosynthetic rates on decadal time scales, time-series analysis of ocean transparency data suggest long-term trends have occurred in the North Pacific Ocean in the 20th century. However, calculations of net carbon uptake by the oceans resulting from phytoplankton photosynthesis suggest that without a supply of nutrients external to the ocean, carbon fixation in the open ocean is not presently a significant sink for excess atmospheric CO₂.The submitted paper has been authored under Contract No. DE-AC02-76H00016 with the US Department of Energy. Accordingly, the US Government retains a non-exclusive, royalty-free license to publish or reproduce the published form of this contribution, or allow others to do so, for US Government purposes.     

Quality–quantity trade‐offs drive functional trait evolution in a model microalgal ‘climate change winner’

Phytoplankton are the unicellular photosynthetic microbes that form the base of aquatic ecosystems, and their responses to global change will impact everything from food web dynamics to global nutrient cycles. Some taxa respond to environmental change by increasing population growth rates in the short‐term and are projected to increase in frequency over decades. To gain insight into how these projected ‘climate change winners’ evolve, we grew populations of microalgae in ameliorated environments for several hundred generations. Most populations evolved to allocate a smaller proportion of carbon to growth while increasing their ability to tolerate and metabolise reactive oxygen species (ROS). This trade‐off drives the evolution of traits that underlie the ecological and biogeochemical roles of phytoplankton. This offers evolutionary and a metabolic frameworks for understanding trait evolution in projected ‘climate change winners’ and suggests that short‐term population booms have the potential to be dampened or reversed when environmental amelioration persists.     

Aluminum effects on marine phytoplankton: implications for a revised Iron Hypothesis (Iron–Aluminum Hypothesis)

In contrast to substantial studies and established knowledge of aluminum (Al) effects (mainly toxicity) on freshwater organisms and terrestrial plants, and even on human health, only a few studies of Al effects on marine organisms have been reported, and our understanding of the role of Al in marine biogeochemistry is limited. In this paper, we review the results of both field and laboratory experiments on the effects of Al on marine organisms, including Al toxicity to marine phytoplankton and the beneficial effects of Al on marine phytoplankton growth, and we discuss possible links of Al to the biological pump and the global carbon cycle. We propose a revised Iron (Fe) Hypothesis, i.e., the Fe–Al Hypothesis that introduces the idea that Al as well as Fe play an important role in the glacial-interglacial change in atmospheric CO₂ concentrations and climate change. We propose that Al could not only facilitate Fe utilization, dissolved organic phosphorus utilization and nitrogen fixation by marine phytoplankton, enhancing phytoplankton biomass and carbon fixation in the upper oceans, but also reduce the decomposition and decay of biogenic matter. As a result, Al allows potentially more carbon to be exported and sequestered in the ocean depths through the biological pump. We also propose that Al binds to superoxide to form an Al-superoxide complex, which could catalyze the reduction of Fe(III) to Fe(II) and thus facilitate Fe utilization by marine phytoplankton and other microbes. Further ocean fertilization experiments with Fe and Al are suggested, to clarify the role of Al in the stimulation of phytoplankton growth and carbon sequestration in the ocean depths.     

Viral attack exacerbates the susceptibility of a bloom‐forming alga to ocean acidification

Both ocean acidification and viral infection bring about changes in marine phytoplankton physiological activities and community composition. However, little information is available on how the relationship between phytoplankton and viruses may be affected by ocean acidification and what impacts this might have on photosynthesis‐driven marine biological CO₂ pump. Here, we show that when the harmful bloom alga Phaeocystis globosa is infected with viruses under future ocean conditions, its photosynthetic performance further decreased and cells became more susceptible to stressful light levels, showing enhanced photoinhibition and reduced carbon fixation, up‐regulation of mitochondrial respiration and decreased virus burst size. Our results indicate that ocean acidification exacerbates the impacts of viral attack on P. globosa, which implies that, while ocean acidification directly influences marine primary producers, it may also affect them indirectly by altering their relationship with viruses. Therefore, viruses as a biotic stressor need to be invoked when considering the overall impacts of climate change on marine productivity and carbon sequestration.     

Sulfur and primary production in aquatic environments: an ecological perspective

Sulfur is one of the critical elements in living matter, as it participates in several structural, metabolic and catalytic activities. Photosynthesis is an important process that entails the use of sulfur during both the light and carbon reactions. Nearly half of global photosynthetic carbon fixation is carried out by phytoplankton in the aquatic environment. Aquatic environments are very different from one another with respect to sulfur content: while in the oceans sulfate concentration is constantly high, freshwaters are characterized by daily and seasonal variations and by a wide range of sulfur concentration. The strategies that algal cells adopt for energy and resource allocation often reflect these differences. In the oceans, the amount and chemical form of sulfur has changed substantially during the course of the Earth's history; it is possible that sulfur availability played a role in the evolution of marine phytoplankton communities and it may continue to have appreciable effects on global biogeochemistry and ecology. Phytoplankton is also the main biogenic source of sulfur; sulfur can be released into the atmosphere by algal cells as dimethylsulfide, with possibly important repercussions on global climate. These and related matters are discussed in this review.     

Global distribution of a wild alga revealed by targeted metagenomics

Eukaryotic phytoplankton play key roles in atmospheric CO(2) uptake and sequestration in marine environments [1,2]. Community shifts attributed to climate change have already been reported in the Arctic ocean, where tiny, photosynthetic picoeukaryotes (≤3 μm diameter) have increased, while larger taxa have decreased [3]. Unfortunately, for vast regions of the world's oceans, little is known about distributions of different genera and levels of genetic variation between ocean basins. This lack of baseline information makes it impossible to assess the impacts of environmental change on phytoplankton diversity, and global carbon cycling. A major knowledge impediment is that these organisms are highly diverse, and most remain uncultured [2]. Metagenomics avoids the culturing step and provides insights into genes present in the environment without some of the biases associated with conventional molecular survey methods. However, connecting metagenomic sequences to the organisms containing them is challenging. For many unicellular eukaryotes the reference genomes needed to make this connection are not available. We circumvented this problem using at-sea fluorescence activated cell sorting (FACS) to separate abundant natural populations of photosynthetic eukaryotes and sequence their DNA, generating reference genome information while eliminating the need for culturing [2]. Here, we present the complete chloroplast genome from an Atlantic picoeukaryote population and discoveries it enabled on the evolution, distribution, and potential carbon sequestration role of a tiny, wild alga.     

Short-term variations in the physiological state of phytoplankton [2pt] in a shallow temperate estuary

Short-term changes in the photosynthetic carbon metabolism and physiological state of phytoplankton were studied over a summer fortnight-long period in the Urdaibai estuary (Bay of Biscay) and related to observed environmental patterns. Day-to-day variability in the hydrographical and biological features of the estuary during the study period was due to changes in meteorological and tidal conditions. Phytoplankton biomass and primary production increased with the improvement of weather, i.e., light conditions, during neap tides. Thus a mixed bloom of cryptophyceans, Euglena sp., and the dinoflagellate Peridinium foliaceum developed in the middle and upper estuary. Photosynthetic responses of phytoplankton were related to the time-scale of changes in light regime. Allocation of photosynthate to major macromolecular classes (LMWM, lipid, polysaccharide, and protein), like phytoplankton biomass and primary production, showed strong spatio-temporal variability. High carbon fixation into low molecular weight metabolites was associated with growth limitation by low light. The relative incorporation of photosynthetic carbon into proteins increased at the beginning of the phytoplankton bloom but overall, it was rather constant. However, carbon allocation into storage products such us lipid or polysaccharide increased when carbon and energy produced under optimal growth conditions exceeded what could be assimilated into protein. These patterns are explained by both spatio-temporal changes in the environmental conditions and species-specific differences. In general, daily variability appeared to be more important than diurnal periodicity in the physiological responses of phytoplankton. Results from this study show that phytoplankton photosynthesis and carbon metabolism are simultaneously affected by biotic and abiotic factors, although short-term light fluctuations may have a major influence on the physiological state of phytoplankton in the Urdaibai estuary.     

Efficient CO2 fixation by surface Prochlorococcus in the Atlantic Ocean

Nearly half of the Earth''s surface is covered by the ocean populated by the most abundant photosynthetic organisms on the planet—Prochlorococcus cyanobacteria. However, in the oligotrophic open ocean, the majority of their cells in the top half of the photic layer have levels of photosynthetic pigmentation barely detectable by flow cytometry, suggesting low efficiency of CO₂ fixation compared with other phytoplankton living in the same waters. To test the latter assumption, CO₂ fixation rates of flow cytometrically sorted ¹⁴C-labelled phytoplankton cells were directly compared in surface waters of the open Atlantic Ocean (30°S to 30°N). CO₂ fixation rates of Prochlorococcus are at least 1.5–2.0 times higher than CO₂ fixation rates of the smallest plastidic protists and Synechococcus cyanobacteria when normalised to photosynthetic pigmentation assessed using cellular red autofluorescence. Therefore, our data indicate that in oligotrophic oceanic surface waters, pigment minimisation allows Prochlorococcus cells to harvest plentiful sunlight more effectively than other phytoplankton.     

Predicting substrate exchange in marine diatom-heterocystous cyanobacteria symbioses

In the open ocean, some phytoplankton establish symbiosis with cyanobacteria. Some partnerships involve diatoms as hosts and heterocystous cyanobacteria as symbionts. Heterocysts are specialized cells for nitrogen fixation, and a function of the symbiotic cyanobacteria is to provide the host with nitrogen. However, both partners are photosynthetic and capable of carbon fixation, and the possible metabolites exchanged and mechanisms of transfer are poorly understood. The symbiont cellular location varies from internal to partial to fully external, and this is reflected in the symbiont genome size and content. In order to identify the membrane transporters potentially involved in metabolite exchange, we compare the draft genomes of three differently located symbionts with known transporters mainly from model free-living heterocystous cyanobacteria. The types and numbers of transporters are directly related to the symbiont cellular location: restricted in the endosymbionts and wider in the external symbiont. Three proposed models of metabolite exchange are suggested which take into account the type of transporters in the symbionts and the influence of their cellular location on the available nutrient pools. These models provide a basis for several hypotheses that given the importance of these symbioses in global N and C budgets, warrant future testing.     

氮输入对滨海盐沼湿地碳循环关键过程的影响及机制

滨海盐沼湿地是缓解全球变暖的有效蓝色碳汇, 但是近岸海域富营养化导致的大量氮输入对盐沼湿地稳定性和碳汇功能构成严重威胁。潮汐作用下大量氮输入对盐沼湿地植物光合碳输入、植物-土壤碳分配和土壤碳输出等碳循环关键过程产生深刻影响, 进而影响盐沼湿地碳汇功能评估的准确性。该文从植物光合固碳、植物-土壤系统碳分配、土壤有机碳分解、土壤可溶性有机碳释放、盐沼湿地土壤碳库5个方面综述了氮输入对盐沼湿地碳循环关键过程的影响。在此基础上, 针对当前研究的不足, 提出今后的研究中, 需要进一步探究氮输入对盐沼湿地植物光合固碳及碳分配过程的影响、盐沼湿地土壤有机碳分解的微生物机制、盐沼湿地土壤可溶性有机碳产生和横向流动的影响、以及氮类型对盐沼湿地土壤碳库的影响。以期为揭示氮输入对盐沼湿地碳汇形成过程与机制提供基础资料和理论依据, 为评估未来近岸海域水体富营养化影响下滨海盐沼湿地碳库的潜在变化提供新思路。     

The Dinoflagellate Lingulodinium polyedrum Responds to N Depletion by a Polarized Deposition of Starch and Lipid Bodies

Dinoflagellates are important contributors to the marine phytoplankton and global carbon fixation, but are also infamous for their ability to form the spectacular harmful algal blooms called red tides. While blooms are often associated with high available nitrogen, there are instances where they are observed in oligotrophic environments. In order to maintain their massive population in conditions of nitrogen limitation, dinoflagellates must have evolved efficient adaptive mechanisms. Here we report the physiological responses to nitrogen deprivation in Lingulodinium polyedrum. We find that this species reacts to nitrogen stress, as do most plants and microalgae, by stopping cell growth and diminishing levels of internal nitrogen, in particular in the form of protein and chlorophyll. Photosynthesis is maintained at high levels for roughly a week following nitrate depletion, resulting in accumulated photosynthetic products in the form of starch. During the second week, photosynthesis rates decrease due to a reduction in the number of chloroplasts and the accumulation of neutral lipid droplets. Surprisingly, the starch granules and lipid droplets are seen to accumulate at opposite poles of the cell. Lastly, we observe that cells acclimated to nitrogen-depleted conditions resume normal growth after addition of inorganic nitrogen, but are able to maintain high cell densities far longer than cells grown continuously in nitrogen-replete conditions.     

单细胞原生生物在海洋碳汇研究中的重要性和展望

海洋是地球上最大的碳库,通过对CO~2的固定以及与大气物质和能量的交换,海洋对全球气候的变化起到关键的调控作用。随着全球气候变化的加剧,增加海洋碳汇已经成为应对全球气候变化的热门研究课题和主要途径之一。海洋微型生物在海洋的固碳过程及碳循环中起到关键的作用,对海洋碳汇意义重大。本文综述了一类重要的海洋微型生物——单细胞原生生物在海洋碳汇研究中的重要性,分析了其中的代表——网粘菌门(Labyrintholomycota)原生生物在海洋碳循环和次级生产中的意义,并从清楚地认识海洋碳汇的过程和机制方面,提出未来该领域急需解决的科学问题和可能的研究方案,为丰富海洋碳汇研究的生物学基础提供理论依据。     

Surplus photosynthetic antennae complexes underlie diagnostics of iron limitation in a cyanobacterium

Chlorophyll fluorescence from phytoplankton provides a tool to assess iron limitation in the oceans, but the physiological mechanism underlying the fluorescence response is not understood. We examined fluorescence properties of the model cyanobacterium Synechocystis PCC6803 and a ΔisiA knock-out mutant of the same species grown under three culture conditions which simulate nutrient conditions found in the open ocean: (1) nitrate and iron replete, (2) limiting-iron and high-nitrate, representative of natural high-nitrate, low-chlorophyll regions, and (3) iron and nitrogen co-limiting. We show that low variable fluorescence, a key diagnostic of iron limitation, results from synthesis of antennae complexes far in excess of what can be accommodated by the iron-restricted pool of photosynthetic reaction centers. Under iron and nitrogen co-limiting conditions, there are no excess antennae complexes and variable fluorescence is high. These results help to explain the well-established fluorescence characteristics of phytoplankton in high-nutrient, low-chlorophyll ocean regions, while also accounting for the lack of these properties in low-iron, low-nitrogen regions. Importantly, our results complete the link between unique molecular consequences of iron stress in phytoplankton and global detection of iron stress in natural populations from space.     

EVOLUTIONARY RESPONSES OF A COCCOLITHOPHORID GEPHYROCAPSA OCEANICA TO OCEAN ACIDIFICATION

The ongoing ocean acidification associated with a changing carbonate system may impose profound effects on marine planktonic calcifiers. Here, we show that a coccolithophore, Gephyrocapsa oceanica, evolved in response to an elevated CO₂ concentration of 1000 μatm (pH reduced to 7.8) in a long‐term (～670 generations) selection experiment. The high CO₂‐selected cells showed increases in photosynthetic carbon fixation, growth rate, cellular particulate organic carbon (POC) or nitrogen (PON) production, and a decrease in C:N elemental ratio, indicating a greater upregulation of PON than of POC production under the ocean acidification condition. Cells from the low CO₂ selection process shifted to high CO₂ exposure showed an enhanced cellular POC and PON production rates. Our data suggest that the coccolithophorid could adapt to ocean acidification with enhanced assimilations of carbon and nitrogen but decreased C:N ratios.     

Interaction of the coccolithophore Gephyrocapsa oceanica with its carbon environment: response to a recreated high-CO2 geological past

Coccolithophores have played a key role in the carbon cycle since becoming dominant in the Cretaceous ocean, and their influence depends fundamentally on how they interact with their external carbon environment. Because the photosynthetic carbon-fixing enzyme Rubisco requires high levels of CO(2) for effective catalysis, coccolithophores are known to induce carbon concentrating mechanisms (CCMs) to raise the level of dissolved inorganic carbon (DIC) in an 'internal pool'. The ocean carbon system has varied greatly over the geological past, suggesting that coccolithophore interactions with that external carbon environment will have changed in parallel. The widespread present-day coccolithophore Gephyrocapsa oceanica was acclimated here to a geological scale change in the seawater carbon system (five times higher DIC and alkalinity). Significant acclimation in response to the external carbon environment was demonstrated by a fourfold increase in the K(m) substrate concentration requirement for half-maximum photosynthetic carbon fixation rates (suggesting that CCMs were down-regulated when ambient carbon was more available). There was, however, no difference in growth rate, morphology or calcification, suggesting that calcification is not coupled to photosynthesis as one of the CCMs induced here and that productivity (growth rate and calcification) is not carbon-limited under representative present-day conditions. Beyond the kinetic parameters of photosynthesis, the only other indication of changed cell physiology seen was the increased fractionation of carbon isotopes into organic matter. These findings demonstrate that G. oceanica changes its carbon-use physiology to maintain consistent photosynthetic carbon fixation in concert with different levels of ambient DIC without changing its morphology or calcification.     

Human-induced salinity changes impact marine organisms and ecosystems

Climate change is fundamentally altering marine and coastal ecosystems on a global scale. While the effects of ocean warming and acidification on ecology and ecosystem functions and services are being comprehensively researched, less attention is directed toward understanding the impacts of human-driven ocean salinity changes. The global water cycle operates through water fluxes expressed as precipitation, evaporation, and freshwater runoff from land. Changes to these in turn modulate ocean salinity and shape the marine and coastal environment by affecting ocean currents, stratification, oxygen saturation, and sea level rise. Besides the direct impact on ocean physical processes, salinity changes impact ocean biological functions with the ecophysiological consequences are being poorly understood. This is surprising as salinity changes may impact diversity, ecosystem and habitat structure loss, and community shifts including trophic cascades. Climate model future projections (of end of the century salinity changes) indicate magnitudes that lead to modification of open ocean plankton community structure and habitat suitability of coral reef communities. Such salinity changes are also capable of affecting the diversity and metabolic capacity of coastal microorganisms and impairing the photosynthetic capacity of (coastal and open ocean) phytoplankton, macroalgae, and seagrass, with downstream ramifications on global biogeochemical cycling. The scarcity of comprehensive salinity data in dynamic coastal regions warrants additional attention. Such datasets are crucial to quantify salinity-based ecosystem function relationships and project such changes that ultimately link into carbon sequestration and freshwater as well as food availability to human populations around the globe. It is critical to integrate vigorous high-quality salinity data with interacting key environmental parameters (e.g., temperature, nutrients, oxygen) for a comprehensive understanding of anthropogenically induced marine changes and its impact on human health and the global economy.