Persistent equatorial Pacific iron limitation under ENSO forcing.

Projected responses of ocean net primary productivity to climate change are highly uncertain1. Models suggest that the climate sensitivity of phytoplankton nutrient limitation in the low-latitude Pacific Ocean plays a crucial role1-3, but this is poorly constrained by observations4. Here we show that changes in physical forcing drove coherent fluctuations in the strength of equatorial Pacific iron limitation through multiple El Niño/Southern Oscillation (ENSO) cycles, but that this was overestimated twofold by a state-of-the-art climate model. Our assessment was enabled by first using a combination of field nutrient-addition experiments, proteomics and above-water hyperspectral radiometry to show that phytoplankton physiological responses to iron limitation led to approximately threefold changes in chlorophyll-normalized phytoplankton fluorescence. We then exploited the >18-year satellite fluorescence record to quantify climate-induced nutrient limitation variability. Such synoptic constraints provide a powerful approach for benchmarking the realism of model projections of net primary productivity to climate changes.

Global analysis of ocean phytoplankton nutrient limitation reveals high prevalence of co-limitation.

Nutrient availability limits phytoplankton growth throughout much of the global ocean. Here we synthesize available experimental data to identify three dominant nutrient limitation regimes: nitrogen is limiting in the stratified subtropical gyres and in the summertime Arctic Ocean, iron is most commonly limiting in upwelling regions, and both nutrients are frequently co-limiting in regions in between the nitrogen and iron limited systems. Manganese can be co-limiting with iron in parts of the Southern Ocean, whilst phosphate and cobalt can be co-/serially limiting in some settings. Overall, an analysis of experimental responses showed that phytoplankton net growth can be significantly enhanced through increasing the number of different nutrients supplied, regardless of latitude, temperature, or trophic status, implying surface seawaters are often approaching nutrient co-limitation. Assessments of nutrient deficiency based on seawater nutrient concentrations and nutrient stress diagnosed via molecular biomarkers showed good agreement with experimentally-assessed nutrient limitation, validating conceptual and theoretical links between nutrient stoichiometry and microbial ecophysiology.

The role of seabird guano in maintaining North Atlantic summertime productivity.

Nutrients supplied via seabird guano increase primary production in some coastal ecosystems. A similar process may occur in the open ocean. To investigate this directly, we first measured bulk and leachable nutrient concentrations in guano sampled in the North Atlantic. We found that guano was strongly enriched in phosphorus, which was released as phosphate in solution. Nitrogen release was dominated by reduced forms (ammonium and urea) whilst release of nitrate was relatively low. A range of trace elements, including the micronutrient iron, were released. Using in-situ bioassays, we then showed that supply of fresh guano to ambient seawater increases phytoplankton biomass and photochemical efficiencies. Based on these results, modelled seabird distributions, and known defecation rates, we estimate that on annual scales guano is a minor source of nutrients for the surface North Atlantic. However, on shorter timescales in late spring/summer it could be much more important: Estimates of upper-level depositions of phosphorus by seabirds were three orders of magnitude higher than modelled aerosol deposition and comparable to diffusion from deeper waters.

Phosphorus Limitation Enhances Diazotroph Zinc Quotas.

Trichodesmium spp. is a colonial diazotrophic cyanobacterium found in the oligotrophic (sub)tropical oceans, where dissolved inorganic phosphorus (DIP) can be depleted. To cope with low P concentrations, P can be scavenged from the dissolved organic P (DOP) pool. This requires the deployment of multiple enzymes activated by trace metals, potentially enhancing metal requirements under stronger P limitations. To test this, we grew Trichodesmium under trace-metal-controlled conditions, where P was supplied as either DIP or DOP (methylphosphonic acid). Mean steady-state biomass under the DOP treatment was only 40% of that grown under equivalent DIP supply, carbon normalized alkaline phosphorus activity was elevated 4-fold, and the zinc (Zn)-carbon ratio was elevated 3.5-fold. Our finding matches the known, dominant Zn requirement across a diversity of enzymes involved in P stress responses and supports an important interaction in the oceanic cycles of these two nutrients.

Exploring Variability of Trichodesmium Photophysiology Using Multi-Excitation Wavelength Fast Repetition Rate Fluorometry.

Fast repetition rate fluorometry (FRRf) allows for rapid non-destructive assessment of phytoplankton photophysiology in situ yet has rarely been applied to Trichodesmium. This gap reflects long-standing concerns that Trichodesmium (and other cyanobacteria) contain pigments that are less effective at absorbing blue light which is often used as the sole excitation source in FRR fluorometers-potentially leading to underestimation of key fluorescence parameters. In this study, we use a multi-excitation FRR fluorometer (equipped with blue, green, and orange LEDs) to investigate photophysiological variability in Trichodesmium assemblages from two sites. Using a multi-LED measurement protocol (447+519+634 nm combined), we assessed maximum photochemical efficiency (F v /F m ), functional absorption cross section of PSII (σ PSII ), and electron transport rates (ETRs) for Trichodesmium assemblages in both the Northwest Pacific (NWP) and North Indian Ocean in the vicinity of Sri Lanka (NIO-SL). Evaluating fluorometer performance, we showed that use of a multi-LED measuring protocol yields a significant increase of F v /F m for Trichodesmium compared to blue-only excitation. We found distinct photophysiological differences for Trichodesmium at both locations with higher average F v /F m as well as lower σ PSII and non-photochemical quenching (NPQ NSV ) observed in the NWP compared to the NIO-SL (Kruskal-Wallis t-test df = 1, p < 0.05). Fluorescence light response curves (FLCs) further revealed differences in ETR response with a lower initial slope (α ETR ) and higher maximum electron turnover rate ( E T R P S I I m a x ) observed for Trichodesmium in the NWP compared to the NIO-SL, translating to a higher averaged light saturation E K (= E T R P S I I m a x /α ETR ) for cells at this location. Spatial variations in physiological parameters were both observed between and within regions, likely linked to nutrient supply and physiological stress. Finally, we applied an algorithm to estimate primary productivity of Trichodesmium using FRRf-derived fluorescence parameters, yielding an estimated carbon-fixation rate ranging from 7.8 to 21.1 mgC mg Chl-a-1 h-1 across this dataset. Overall, our findings demonstrate that capacity of multi-excitation FRRf to advance the application of Chl-a fluorescence techniques in phytoplankton assemblages dominated by cyanobacteria and reveals novel insight into environmental regulation of photoacclimation in natural Trichodesmium populations.

Nutrient regulation of biological nitrogen fixation across the tropical western North Pacific.

Nitrogen fixation is critical for the biological productivity of the ocean, but clear mechanistic controls on this process remain elusive. Here, we investigate the abundance, activity, and drivers of nitrogen-fixing diazotrophs across the tropical western North Pacific. We find a basin-scale coherence of diazotroph abundances and N2 fixation rates with the supply ratio of iron:nitrogen to the upper ocean. Across a threshold of increasing supply ratios, the abundance of nifH genes and N2 fixation rates increased, phosphate concentrations decreased, and bioassay experiments demonstrated evidence for N2 fixation switching from iron to phosphate limitation. In the northern South China Sea, supply ratios were hypothesized to fall around this critical threshold and bioassay experiments suggested colimitation by both iron and phosphate. Our results provide evidence for iron:nitrogen supply ratios being the most important factor in regulating the distribution of N2 fixation across the tropical ocean.

Manganese co-limitation of phytoplankton growth and major nutrient drawdown in the Southern Ocean.

Residual macronutrients in the surface Southern Ocean result from restricted biological utilization, caused by low wintertime irradiance, cold temperatures, and insufficient micronutrients. Variability in utilization alters oceanic CO2 sequestration at glacial-interglacial timescales. The role for insufficient iron has been examined in detail, but manganese also has an essential function in photosynthesis and dissolved concentrations in the Southern Ocean can be strongly depleted. However, clear evidence for or against manganese limitation in this system is lacking. Here we present results from ten experiments distributed across Drake Passage. We found manganese (co-)limited phytoplankton growth and macronutrient consumption in central Drake Passage, whilst iron limitation was widespread nearer the South American and Antarctic continental shelves. Spatial patterns were reconciled with the different rates and timescales for removal of each element from seawater. Our results suggest an important role for manganese in modelling Southern Ocean productivity and understanding major nutrient drawdown in glacial periods.

The influence of Arctic Fe and Atlantic fixed N on summertime primary production in Fram Strait, North Greenland Sea.

Climate change has led to a ~ 40% reduction in summer Arctic sea-ice cover extent since the 1970s. Resultant increases in light availability may enhance phytoplankton production. Direct evidence for factors currently constraining summertime phytoplankton growth in the Arctic region is however lacking. GEOTRACES cruise GN05 conducted a Fram Strait transect from Svalbard to the NE Greenland Shelf in summer 2016, sampling for bioessential trace metals (Fe, Co, Zn, Mn) and macronutrients (N, Si, P) at ~ 79°N. Five bioassay experiments were conducted to establish phytoplankton responses to additions of Fe, N, Fe + N and volcanic dust. Ambient nutrient concentrations suggested N and Fe were deficient in surface seawater relative to typical phytoplankton requirements. A west-to-east trend in the relative deficiency of N and Fe was apparent, with N becoming more deficient towards Greenland and Fe more deficient towards Svalbard. This aligned with phytoplankton responses in bioassay experiments, which showed greatest chlorophyll-a increases in + N treatment near Greenland and + N + Fe near Svalbard. Collectively these results suggest primary N limitation of phytoplankton growth throughout the study region, with conditions potentially approaching secondary Fe limitation in the eastern Fram Strait. We suggest that the supply of Atlantic-derived N and Arctic-derived Fe exerts a strong control on summertime nutrient stoichiometry and resultant limitation patterns across the Fram Strait region.

Heme b distributions through the Atlantic Ocean: evidence for "anemic" phytoplankton populations.

Heme b is an iron-containing cofactor in hemoproteins that participates in the fundamental processes of photosynthesis and respiration in phytoplankton. Heme b concentrations typically decline in waters with low iron concentrations but due to lack of field data, the distribution of heme b in particulate material in the ocean is poorly constrained. Here we report particulate heme b distributions across the Atlantic Ocean (59.9°N to 34.6°S). Heme b concentrations in surface waters ranged from 0.10 to 33.7 pmol L-1 (median = 1.47 pmol L-1, n = 974) and were highest in regions with a high biomass. The ratio of heme b to particulate organic carbon (POC) exhibited a mean value of 0.44 µmol heme b mol-1 POC. We identified the ratio of 0.10 µmol heme b mol-1 POC as the cut-off between heme b replete and heme b deficient (anemic) phytoplankton. By this definition, we observed anemic phytoplankton populations in the Subtropical South Atlantic and Irminger Basin. Comparison of observed and modelled heme b suggested that heme b could account for between 0.17-9.1% of biogenic iron. Our large scale observations of heme b relative to organic matter provide further evidence of the impact of changes in iron supply on phytoplankton iron status across the Atlantic Ocean.

Regulation of the Phytoplankton Heme b Iron Pool During the North Atlantic Spring Bloom.

Heme b is an iron-containing co-factor in hemoproteins. Heme b concentrations are low (<1 pmol L-1) in iron limited phytoplankton in cultures and in the field. Here, we determined heme b in marine particulate material (>0.7 µm) from the North Atlantic Ocean (GEOVIDE cruise - GEOTRACES section GA01), which spanned several biogeochemical regimes. We examined the relationship between heme b abundance and the microbial community composition, and its utility for mapping iron limited phytoplankton. Heme b concentrations ranged from 0.16 to 5.1 pmol L-1 (median = 2.0 pmol L-1, n = 62) in the surface mixed layer (SML) along the cruise track, driven mainly by variability in biomass. However, in the Irminger Basin, the lowest heme b levels (SML: median = 0.53 pmol L-1, n = 12) were observed, whilst the biomass was highest (particulate organic carbon, median = 14.2 µmol L-1, n = 25; chlorophyll a: median = 2.0 nmol L-1, n = 23) pointing to regulatory mechanisms of the heme b pool for growth conservation. Dissolved iron (DFe) was not depleted (SML: median = 0.38 nmol L-1, n = 11) in the Irminger Basin, but large diatoms (Rhizosolenia sp.) dominated. Hence, heme b depletion and regulation is likely to occur during bloom progression when phytoplankton class-dependent absolute iron requirements exceed the available ambient concentration of DFe. Furthermore, high heme b concentrations found in the Iceland Basin and Labrador Sea (median = 3.4 pmol L-1, n = 20), despite having similar DFe concentrations to the Irminger Basin, were attributed to an earlier growth phase of the extant phytoplankton populations. Thus, heme b provides a snapshot of the cellular activity in situ and could both be used as indicator of iron limitation and contribute to understanding phytoplankton adaptation mechanisms to changing iron supplies.

Publisher Correction: Marine microbial metagenomes sampled across space and time.

Due to a typesetting error, 25 rows were omitted from Table 3 in the original version of this Data Descriptor. These missing rows correspond to the following sample names.

Single cell genomes of Prochlorococcus, Synechococcus, and sympatric microbes from diverse marine environments.

Prochlorococcus and Synechococcus are the dominant primary producers in marine ecosystems and perform a significant fraction of ocean carbon fixation. These cyanobacteria interact with a diverse microbial community that coexists with them. Comparative genomics of cultivated isolates has helped address questions regarding patterns of evolution and diversity among microbes, but the fraction that can be cultivated is miniscule compared to the diversity in the wild. To further probe the diversity of these groups and extend the utility of reference sequence databases, we report a data set of single cell genomes for 489 Prochlorococcus, 50 Synechococcus, 9 extracellular virus particles, and 190 additional microorganisms from a diverse range of bacterial, archaeal, and viral groups. Many of these uncultivated single cell genomes are derived from samples obtained on GEOTRACES cruises and at well-studied oceanographic stations, each with extensive suites of physical, chemical, and biological measurements. The genomic data reported here greatly increases the number of available Prochlorococcus genomes and will facilitate studies on evolutionary biology, microbial ecology, and biological oceanography.

Marine microbial metagenomes sampled across space and time.

Recent advances in understanding the ecology of marine systems have been greatly facilitated by the growing availability of metagenomic data, which provide information on the identity, diversity and functional potential of the microbial community in a particular place and time. Here we present a dataset comprising over 5 terabases of metagenomic data from 610 samples spanning diverse regions of the Atlantic and Pacific Oceans. One set of metagenomes, collected on GEOTRACES cruises, captures large geographic transects at multiple depths per station. The second set represents two years of time-series data, collected at roughly monthly intervals from 3 depths at two long-term ocean sampling sites, Station ALOHA and BATS. These metagenomes contain genomic information from a diverse range of bacteria, archaea, eukaryotes and viruses. The data's utility is strengthened by the availability of extensive physical, chemical, and biological measurements associated with each sample. We expect that these metagenomes will facilitate a wide range of comparative studies that seek to illuminate new aspects of marine microbial ecosystems.

Nutrient co-limitation at the boundary of an oceanic gyre.

Nutrient limitation of oceanic primary production exerts a fundamental control on marine food webs and the flux of carbon into the deep ocean. The extensive boundaries of the oligotrophic sub-tropical gyres collectively define the most extreme transition in ocean productivity, but little is known about nutrient limitation in these zones. Here we present the results of full-factorial nutrient amendment experiments conducted at the eastern boundary of the South Atlantic gyre. We find extensive regions in which the addition of nitrogen or iron individually resulted in no significant phytoplankton growth over 48 hours. However, the addition of both nitrogen and iron increased concentrations of chlorophyll a by up to approximately 40-fold, led to diatom proliferation, and reduced community diversity. Once nitrogen-iron co-limitation had been alleviated, the addition of cobalt or cobalt-containing vitamin B12 could further enhance chlorophyll a yields by up to threefold. Our results suggest that nitrogen-iron co-limitation is pervasive in the ocean, with other micronutrients also approaching co-deficiency. Such multi-nutrient limitations potentially increase phytoplankton community diversity.

Mechanisms of silver nanoparticle toxicity to the coastal marine diatom Chaetoceros curvisetus.

Inputs of silver nanoparticles (AgNPs) to marine waters continue to increase yet mechanisms of AgNPs toxicity to marine phytoplankton are still not well resolved. This study reports a series of toxicity experiments on a representative coastal marine diatom species Chaetoceros curvisetus using the reference AgNP, NM-300K. Exposure to AgNPs resulted in photosynthetic impairment and loss of diatom biomass in proportion to the supplied AgNP dose. The underlying mechanism of toxicity was explored via comparing biological responses in parallel experiments. Diatom responses to AgNP, free Ag(I) species, and dialysis bag-retained AgNP treatments showed marked similarity, pointing towards a dominant role of Ag(I) species uptake, rather than NPs themselves, in inducing the toxic response. In marked contrast to previous studies, addition of the organic complexing agent cysteine (Cys) alongside Ag only marginally moderated toxicity, implying AgCys- complexes were bioavailable to this diatom species. A preliminary field experiment with a natural phytoplankton community in the southeast Atlantic Ocean showed no significant toxic response at a NM-300 K concentration that resulted in ~40% biomass loss in the culture studies, suggesting a modulating effect of natural seawaters on Ag toxicity.