Phytoplankton responses to changing temperature and nutrient availability are consistent across the tropical and subtropical Atlantic.

Temperature and nutrient supply interactively control phytoplankton growth and productivity, yet the role of these drivers together still has not been determined experimentally over large spatial scales in the oligotrophic ocean. We conducted four microcosm experiments in the tropical and subtropical Atlantic (29°N-27°S) in which surface plankton assemblages were exposed to all combinations of three temperatures (in situ, 3 °C warming and 3 °C cooling) and two nutrient treatments (unamended and enrichment with nitrogen and phosphorus). We found that chlorophyll a concentration and the biomass of picophytoplankton consistently increase in response to nutrient addition, whereas changes in temperature have a smaller and more variable effect. Nutrient enrichment leads to increased picoeukaryote abundance, depressed Prochlorococcus abundance, and increased contribution of small nanophytoplankton to total biomass. Warming and nutrient addition synergistically stimulate light-harvesting capacity, and accordingly the largest biomass response is observed in the warmed, nutrient-enriched treatment at the warmest and least oligotrophic location (12.7°N). While moderate nutrient increases have a much larger impact than varying temperature upon the growth and community structure of tropical phytoplankton, ocean warming may increase their ability to exploit events of enhanced nutrient availability.

Nitrous oxide and methane in a changing Arctic Ocean.

Human activities are changing the Arctic environment at an unprecedented rate resulting in rapid warming, freshening, sea ice retreat and ocean acidification of the Arctic Ocean. Trace gases such as nitrous oxide (N2O) and methane (CH4) play important roles in both the atmospheric reactivity and radiative budget of the Arctic and thus have a high potential to influence the region's climate. However, little is known about how these rapid physical and chemical changes will impact the emissions of major climate-relevant trace gases from the Arctic Ocean. The combined consequences of these stressors present a complex combination of environmental changes which might impact on trace gas production and their subsequent release to the Arctic atmosphere. Here we present our current understanding of nitrous oxide and methane cycling in the Arctic Ocean and its relevance for regional and global atmosphere and climate and offer our thoughts on how this might change over coming decades.

High spatial resolution global ocean metagenomes from Bio-GO-SHIP repeat hydrography transects.

Detailed descriptions of microbial communities have lagged far behind physical and chemical measurements in the marine environment. Here, we present 971 globally distributed surface ocean metagenomes collected at high spatio-temporal resolution. Our low-cost metagenomic sequencing protocol produced 3.65 terabases of data, where the median number of base pairs per sample was 3.41 billion. The median distance between sampling stations was 26 km. The metagenomic libraries described here were collected as a part of a biological initiative for the Global Ocean Ship-based Hydrographic Investigations Program, or "Bio-GO-SHIP." One of the primary aims of GO-SHIP is to produce high spatial and vertical resolution measurements of key state variables to directly quantify climate change impacts on ocean environments. By similarly collecting marine metagenomes at high spatiotemporal resolution, we expect that this dataset will help answer questions about the link between microbial communities and biogeochemical fluxes in a changing ocean.

Drivers of spectral optical scattering by particles in the upper 500 m of the Atlantic Ocean.

Optical models have been proposed to relate spectral variations in the beam attenuation (cp) and optical backscattering (bbp) coefficients to marine particle size distributions (PSDs). However, due to limited PSD data, particularly in the open ocean, optically derived PSDs suffer from large uncertainties and we have a poor empirical understanding of the drivers of spectral cp and bbp coefficients. Here we evaluated PSD optical proxies and investigated their drivers by analyzing an unprecedented dataset of co-located PSDs, phytoplankton abundances and optical measurements collected across the upper 500 m of the Atlantic Ocean. The spectral slope of cp was correlated (r>0.59) with the slope of the PSD only for particles with diameters >1 µm and also with eukaryotic phytoplankton concentrations. No significant relationships between PSDs and the spectral slope of bbp were observed. In the upper 200 m, the bbp spectral slope was correlated to the light absorption by particles (ap; r<-0.54) and to the ratio of cyanobacteria to eukaryotic phytoplankton. This latter correlation was likely the consequence of the strong relationship we observed between ap and the concentration of eukaryotic phytoplankton (r=0.83).

Radiometric approach for the detection of picophytoplankton assemblages across oceanic fronts.

Cell abundances of Prochlorococcus, Synechococcus, and autotrophic picoeukaryotes were estimated in surface waters using principal component analysis (PCA) of hyperspectral and multispectral remote-sensing reflectance data. This involved the development of models that employed multilinear correlations between cell abundances across the Atlantic Ocean and a combination of PCA scores and sea surface temperatures. The models retrieve high Prochlorococcus abundances in the Equatorial Convergence Zone and show their numerical dominance in oceanic gyres, with decreases in Prochlorococcus abundances towards temperate waters where Synechococcus flourishes, and an emergence of picoeukaryotes in temperate waters. Fine-scale in-situ sampling across ocean fronts provided a large dynamic range of measurements for the training dataset, which resulted in the successful detection of fine-scale Synechococcus patches. Satellite implementation of the models showed good performance (R2 > 0.50) when validated against in-situ data from six Atlantic Meridional Transect cruises. The improved relative performance of the hyperspectral models highlights the importance of future high spectral resolution satellite instruments, such as the NASA PACE mission's Ocean Color Instrument, to extend our spatiotemporal knowledge about ecologically relevant phytoplankton assemblages.

Increasing picocyanobacteria success in shelf waters contributes to long-term food web degradation.

Continental margins are disproportionally important for global primary production, fisheries and CO2 uptake. However, across the Northeast Atlantic shelves, there has been an ongoing summertime decline of key biota-large diatoms, dinoflagellates and copepods-that traditionally fuel higher tropic levels such as fish, sea birds and marine mammals. Here, we combine multiple time series with in situ process studies to link these declines to summer nutrient stress and increasing proportions of picophytoplankton that can comprise up to 90% of the combined pico- and nanophytoplankton biomass in coastal areas. Among the pico-fraction, it is the cyanobacterium Synechococcus that flourishes when iron and nitrogen resupply to surface waters are diminished. Our field data show how traits beyond small size give Synechococcus a competitive edge over pico- and nanoeukaryotes. Key is their ability to grow at low irradiances near the nutricline, which is aided by their superior light-harvesting system and high affinity to iron. However, minute size and lack of essential biomolecules (e.g. omega-3 polyunsaturated fatty acids and sterols) render Synechococcus poor primary producers to sustain shelf sea food webs efficiently. The combination of earlier spring blooms and lower summer food quantity and quality creates an increasing period of suboptimal feeding conditions for zooplankton at a time of year when their metabolic demand is highest. We suggest that this nutrition-related mismatch has contributed to the widespread, ~50% decline in summer copepod abundance we observe over the last 60 years. With Synechococcus clades being prominent from the tropics to the Arctic and their abundances increasing worldwide, our study informs projections of future food web dynamics in coastal and shelf areas where droughts and stratification lead to increasing nutrient starvation of surface waters.

Modulation of Polar Lipid Profiles in Chlorella sp. in Response to Nutrient Limitation.

We evaluate the effects of nutrient limitation on cellular composition of polar lipid classes/species in Chlorella sp. using modern polar lipidomic profiling methods (liquid chromatography⁻tandem mass spectrometry; LC-MS/MS). Total polar lipid concentration was highest in nutrient-replete (HN) cultures with a significant reduction in monogalactosyldiacylglycerol (MGDG), phosphatidylglycerol (PG), phosphatidylcholine (PC), and phosphatidylethanolamine (PE) class concentrations for nutrient-deplete (LN) cultures. Moreover, reductions in the abundance of MGDG relative to total polar lipids versus an increase in the relative abundance of digalactosyldiacylglycerol (DGDG) were recorded in LN cultures. In HN cultures, polar lipid species composition remained relatively constant throughout culture with high degrees of unsaturation associated with acyl moieties. Conversely, in LN cultures lipid species composition shifted towards greater saturation of acyl moieties. Multivariate analyses revealed that changes in the abundance of a number of species contributed to the dissimilarity between LN and HN cultures but with dominant effects from certain species, e.g., reduction in MGDG 34:7 (18:3/16:4). Results demonstrate that Chlorella sp. significantly alters its polar lipidome in response to nutrient limitation, and this is discussed in terms of physiological significance and polar lipids production for applied microalgal production systems.

The open-ocean missing backscattering is in the structural complexity of particles.

Marine microscopic particles profoundly impact global biogeochemical cycles, but our understanding of their dynamics is hindered by lack of observations. To fill this gap, optical backscattering measured by satellite sensors and in-situ autonomous platforms can be exploited. Unfortunately, these observations remain critically limited by an incomplete mechanistic understanding of what particles generate the backscattering signal. To achieve this understanding, optical models are employed. The simplest of these models-the homogeneous sphere-severely underestimates the measured backscattering and the missing signal has been attributed to submicron particles. This issue is known as the missing backscattering enigma. Here we show that a slightly more complex optical model-the coated sphere-can predict the measured backscattering and suggests that most of the signal comes from particles >1 µm. These findings were confirmed by independent size-fractionation experiments. Our results demonstrate that the structural complexity of particles is critical to understand open-ocean backscattering and contribute to solving the enigma.

Basin-Scale Observations of Monoterpenes in the Arctic and Atlantic Oceans.

We report novel in situ speciated observations of monoterpenes (α- and ß-pinene, myrcene, δ3-carene, ocimene, limonene) in seawater and air during three cruises in the Arctic and Atlantic Oceans, in/over generally oligotrophic waters. Oceanic concentrations of the individual monoterpenes ranged from below the detection limit of <1 pmol L-1 to 5 pmol L-1, with average concentrations of between 0.5 and 2.9 pmol L-1. After careful filtering for contamination, atmospheric mixing ratios varied from below the detection limit (<1 pptv) to 5 pptv, with averages of 0.05-5 pptv; these levels are up to 2 orders of magnitude lower than those reported previously. This could be at least partly due to sampling over waters with much lower biological activity than in previous studies. Unlike in previous studies, no clear relationships of the monoterpenes with biological variables were found. Based on our measured seawater concentrations and a global model simulation, we estimate total global marine monoterpene emissions of 0.16 Tg C yr-1, similar to a previous bottom-up estimate based on laboratory monoculture studies but 2 orders of magnitude lower than a previous top-down estimate of 29.5 Tg C yr-1.

Microbial acetone oxidation in coastal seawater.

Acetone is an important oxygenated volatile organic compound (OVOC) in the troposphere where it influences the oxidizing capacity of the atmosphere. However, the air-sea flux is not well quantified, in part due to a lack of knowledge regarding which processes control oceanic concentrations, and, specifically whether microbial oxidation to CO2 represents a significant loss process. We demonstrate that (14)C labeled acetone can be used to determine microbial oxidation to (14)CO2. Linear microbial rates of acetone oxidation to CO2 were observed for between 0.75-3.5 h at a seasonally eutrophic coastal station located in the western English Channel (L4). A kinetic experiment in summer at station L4 gave a V max of 4.1 pmol L(-1) h(-1), with a K m constant of 54 pM. We then used this technique to obtain microbial acetone loss rates ranging between 1.2 and 42 pmol L(-1) h(-1.)(monthly averages) over an annual cycle at L4, with maximum rates observed during winter months. The biological turnover time of acetone (in situ concentration divided by microbial oxidation rate) in surface waters varied from ~3 days in February 2011, when in situ concentrations were 3 ± 1 nM, to >240 days in June 2011, when concentrations were more than twofold higher at 7.5 ± 0.7 nM. These relatively low marine microbial acetone oxidation rates, when normalized to in situ concentrations, suggest that marine microbes preferentially utilize other OVOCs such as methanol and acetaldehyde.

Flow cytometric identification of Mamiellales clade II in the Southern Atlantic Ocean.

Flow cytometric sorting, based on cellular optical properties and macromolecule content, has been successfully employed to taxonomically affiliate bacterioplankton. However, this approach has not been much used for eukaryotic plankton. To redress this imbalance, we identified a conspicuous group of red autofluorescent picoplankton in surface waters of the South Atlantic Ocean. Using catalysed reporter deposition fluorescence in situ hybridization, virtually, all cells sorted from that group were affiliated with the Mamiellales clade II (84 ± 4%, division Chlorophyta) with a size of 1.6 ± 0.03 µm. Based on electron microscopy, the Mamiellales clade II-sorted cells have a simple morphology with apparently no scales, flagella or surface features. Their latitudinal distribution resembled the distribution of Synechococcus with very low concentrations in the surface waters of the Southern subtropical gyre (0.6-1.6 × 10(3) cells mL(-1)) and increased concentrations in the Southern temperate waters 8.3 × 10(3) cells mL(-1). Identification of the flow cytometric group as Mamiellales clade II allowed us to characterize the morphology of these enigmatic uncultured picoplanktonic cells by electron microscopy and to determine their apparent preference for temperate rather than subtropical oceanic photic waters.

Comparable light stimulation of organic nutrient uptake by SAR11 and Prochlorococcus in the North Atlantic subtropical gyre.

Subtropical oceanic gyres are the most extensive biomes on Earth where SAR11 and Prochlorococcus bacterioplankton numerically dominate the surface waters depleted in inorganic macronutrients as well as in dissolved organic matter. In such nutrient poor conditions bacterioplankton could become photoheterotrophic, that is, potentially enhance uptake of scarce organic molecules using the available solar radiation to energise appropriate transport systems. Here, we assessed the photoheterotrophy of the key microbial taxa in the North Atlantic oligotrophic gyre and adjacent regions using (33)P-ATP, (3)H-ATP and (35)S-methionine tracers. Light-stimulated uptake of these substrates was assessed in two dominant bacterioplankton groups discriminated by flow cytometric sorting of tracer-labelled cells and identified using catalysed reporter deposition fluorescence in situ hybridisation. One group of cells, encompassing 48% of all bacterioplankton, were identified as members of the SAR11 clade, whereas the other group (24% of all bacterioplankton) was Prochlorococcus. When exposed to light, SAR11 cells took 31% more ATP and 32% more methionine, whereas the Prochlorococcus cells took 33% more ATP and 34% more methionine. Other bacterioplankton did not demonstrate light stimulation. Thus, the SAR11 and Prochlorococcus groups, with distinctly different light-harvesting mechanisms, used light equally to enhance, by approximately one-third, the uptake of different types of organic molecules. Our findings indicate the significance of light-driven uptake of essential organic nutrients by the dominant bacterioplankton groups in the surface waters of one of the less productive, vast regions of the world's oceans-the oligotrophic North Atlantic subtropical gyre.

Mixotrophic basis of Atlantic oligotrophic ecosystems.

Oligotrophic subtropical gyres are the largest oceanic ecosystems, covering >40% of the Earth's surface. Unicellular cyanobacteria and the smallest algae (plastidic protists) dominate CO(2) fixation in these ecosystems, competing for dissolved inorganic nutrients. Here we present direct evidence from the surface mixed layer of the subtropical gyres and adjacent equatorial and temperate regions of the Atlantic Ocean, collected on three Atlantic Meridional Transect cruises on consecutive years, that bacterioplankton are fed on by plastidic and aplastidic protists at comparable rates. Rates of bacterivory were similar in the light and dark. Furthermore, because of their higher abundance, it is the plastidic protists, rather than the aplastidic forms, that control bacterivory in these waters. These findings change our basic understanding of food web function in the open ocean, because plastidic protists should now be considered as the main bacterivores as well as the main CO(2) fixers in the oligotrophic gyres.

Light scattering by coccoliths detached from Emiliania huxleyi.

We used in situ radiance/irradiance profiles to retrieve profiles of the spectral backscattering coefficient for all particles in an E. huxleyi coccolithophore bloom off the coast of Plymouth, UK. At high detached coccolith concentrations the spectra of backscattering all showed a minimum near approximately 550 to 600 nm. Using flow cytometry estimates of the detached coccolith concentration, and assuming all of the backscattering (over and above the backscattering by the water itself) was due to detached coccoliths, we determined the upper limit of the backscattering cross section (sigma(b)) of individual coccoliths to be 0.123+/-0.039 microm(2)/coccolith at 500 nm. Physical models of detached coccoliths were then developed and the discrete dipole approximation was used to compute their average backscattering cross section in random orientation. The result was 0.092 microm(2) at 500 nm, with the computed sigma(b) displaying a spectral shape similar to the measurements, but with less apparent increase in backscattering toward the red. When sigma(b) is computed on a per mole of calcite, rather than a per coccolith basis, it agreed reasonably well with that determined for acid-labile backscattering at 632 nm averaged over several species of cultured calcifying algae. Intact coccolithophore cells were taken into account by arguing that coccoliths attached to coccolithophore cells (forming a "coccosphere") backscatter in a manner similar to free coccoliths in random orientation. Estimating the number of coccoliths per coccosphere and using the observed number of coccolithophore cells resulted is an apparent backscattering cross section at 500 nm of 0.114+/-0.013 microm(2)/coccolith, in satisfactory agreement with the measured backscattering.

Latitudinal distribution of prokaryotic picoplankton populations in the Atlantic Ocean.

Members of the prokaryotic picoplankton are the main drivers of the biogeochemical cycles over large areas of the world's oceans. In order to ascertain changes in picoplankton composition in the euphotic and twilight zones at an ocean basin scale we determined the distribution of 11 marine bacterial and archaeal phyla in three different water layers along a transect across the Atlantic Ocean from South Africa (32.9 degrees S) to the UK (46.4 degrees N) during boreal spring. Depth profiles down to 500 m at 65 stations were analysed by catalysed reporter deposition fluorescence in situ hybridization (CARD-FISH) and automated epifluorescence microscopy. There was no obvious overall difference in microbial community composition between the surface water layer and the deep chlorophyll maximum (DCM) layer. There were, however, significant differences between the two photic water layers and the mesopelagic zone. SAR11 (35 +/- 9%) and Prochlorococcus (12 +/- 8%) together dominated the surface waters, whereas SAR11 and Crenarchaeota of the marine group I formed equal proportions of the picoplankton community below the DCM (both approximately 15%). However, due to their small cell sizes Crenarchaeota contributed distinctly less to total microbial biomass than SAR11 in this mesopelagic water layer. Bacteria from the uncultured Chloroflexi-related clade SAR202 occurred preferentially below the DCM (4-6%). Distinct latitudinal distribution patterns were found both in the photic zone and in the mesopelagic waters: in the photic zone, SAR11 was more abundant in the Northern Atlantic Ocean (up to 45%) than in the Southern Atlantic gyre (approximately 25%), the biomass of Prochlorococcus peaked in the tropical Atlantic Ocean, and Bacteroidetes and Gammaproteobacteria bloomed in the nutrient-rich northern temperate waters and in the Benguela upwelling. In mesopelagic waters, higher proportions of SAR202 were present in both central gyre regions, whereas Crenarchaeota were clearly more abundant in the upwelling regions and in higher latitudes. Other phylogenetic groups such as the Planctomycetes, marine group II Euryarchaeota and the uncultured clades SAR406, SAR324 and SAR86 rarely exceeded more than 5% of relative abundance.

High bacterivory by the smallest phytoplankton in the North Atlantic Ocean.

Planktonic algae <5 m in size are major fixers of inorganic carbon in the ocean. They dominate phytoplankton biomass in post-bloom, stratified oceanic temperate waters. Traditionally, large and small algae are viewed as having a critical growth dependence on inorganic nutrients, which the latter can better acquire at lower ambient concentrations owing to their higher surface area to volume ratios. Nonetheless, recent phosphate tracer experiments in the oligotrophic ocean have suggested that small algae obtain inorganic phosphate indirectly, possibly through feeding on bacterioplankton. There have been numerous microscopy-based studies of algae feeding mixotrophically in the laboratory and field as well as mathematical modelling of the ecological importance of mixotrophy. However, because of methodological limitations there has not been a direct comparison of obligate heterotrophic and mixotrophic bacterivory. Here we present direct evidence that small algae carry out 40-95% of the bacterivory in the euphotic layer of the temperate North Atlantic Ocean in summer. A similar range of 37-70% was determined in the surface waters of the tropical North-East Atlantic Ocean, suggesting the global significance of mixotrophy. This finding reveals that even the smallest algae have less dependence on dissolved inorganic nutrients than previously thought, obtaining a quarter of their biomass from bacterivory. This has important implications for how we perceive nutrient acquisition and limitation of carbon-fixing protists as well as control of bacterioplankton in the ocean.

Diel rhythmicity in amino acid uptake by Prochlorococcus.

The marine cyanobacterium Prochlorococcus, the most abundant phototrophic organism on Earth, numerically dominates the phytoplankton in nitrogen (N)-depleted oceanic gyres. Alongside inorganic N sources such as nitrite and ammonium, natural populations of this genus also acquire organic N, specifically amino acids. Here, we investigated using isotopic tracer and flow cytometric cell sorting techniques whether amino acid uptake by Prochlorococcus is subject to a diel rhythmicity, and if so, whether this was linked to a specific cell cycle stage. We observed, in contrast to diurnally similar methionine uptake rates by Synechococcus cells, obvious diurnal rhythms in methionine uptake by Prochlorococcus cells in the tropical Atlantic. These rhythms were confirmed using reproducible cyclostat experiments with a light-synchronized axenic Prochlorococcus (PCC9511 strain) culture and (35)S-methionine and (3)H-leucine tracers. Cells acquired the tracers at lower rates around dawn and higher rates around dusk despite >10(4) times higher concentration of ammonium in the medium, presumably because amino acids can be directly incorporated into protein. Leucine uptake rates by cells in the S+G(2) cell cycle stage were consistently 2.2 times higher than those of cells at the G(1) stage. Furthermore, S+G(2) cells upregulated amino acid uptake 3.5 times from dawn to dusk to boost protein synthesis prior to cell division. Because Prochlorococcus populations can account from 13% at midday to 42% at dusk of total microbial uptake of methionine and probably of other amino acids in N-depleted oceanic waters, this genus exerts diurnally variable, strong competitive pressure on other bacterioplankton populations.

Light enhanced amino acid uptake by dominant bacterioplankton groups in surface waters of the Atlantic Ocean.

(35)S-Methionine and (3)H-leucine bioassay tracer experiments were conducted on two meridional transatlantic cruises to assess whether dominant planktonic microorganisms use visible sunlight to enhance uptake of these organic molecules at ambient concentrations. The two numerically dominant groups of oceanic bacterioplankton were Prochlorococcus cyanobacteria and bacteria with low nucleic acid (LNA) content, comprising 60% SAR11-related cells. The results of flow cytometric sorting of labelled bacterioplankton cells showed that when incubated in the light, Prochlorococcus and LNA bacteria increased their uptake of amino acids on average by 50% and 23%, respectively, compared with those incubated in the dark. Amino acid uptake of Synechococcus cyanobacteria was also enhanced by visible light, but bacteria with high nucleic acid content showed no light stimulation. Additionally, differential uptake of the two amino acids by the Prochlorococcus and LNA cells was observed. The populations of these two types of cells on average completely accounted for the determined 22% light enhancement of amino acid uptake by the total bacterioplankton community, suggesting a plausible way of harnessing light energy for selectively transporting scarce nutrients that could explain the numerical dominance of these groups in situ.

Hydroxamate siderophores: occurrence and importance in the Atlantic Ocean.

Siderophores are chelates produced by bacteria as part of a highly specific iron uptake mechanism. They are thought to be important in the bacterial acquisition of iron in seawater and to influence iron biogeochemistry in the ocean. We have identified and quantified two types of siderophores in seawater samples collected from the Atlantic Ocean. These siderophores were identified as hydroxamate siderophores, both ferrioxamine species representative of the more soluble marine siderophores characterized to date. Ferrioxamine G was widely distributed in surface waters throughout the Atlantic Ocean, while ferrioxamine E had a more varied distribution. Total concentrations of the two siderophores were between 3 and 20 pM in the euphotic zone. If these compounds are fully complexed in seawater, they represent approximately 0.2-4.6% of the <0.2 microm iron pool. Our data confirm that siderophore-mediated iron acquisition is important for marine heterotrophic bacteria and indicate that siderophores play an important role in the oceanic biogeochemical cycling of iron.

Dynamics of ribulose 1,5-bisphosphate carboxylase/oxygenase gene expression in the coccolithophorid Coccolithus pelagicus during a tracer release experiment in the Northeast Atlantic.

We report a pronounced diel rhythm in ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO) gene expression in a natural population of the coccolithophorid Coccolithus pelagicus sampled during a Lagrangian experiment in the Northeast Atlantic. Our observations show that there is greater heterogeneity in the temporal regulation of RubisCO expression among planktonic chromophytes than has been reported hitherto.