Coexistence of Dominant Marine Phytoplankton Sustained by Nutrient Specialization.

Prochlorococcus and Synechococcus are the two dominant picocyanobacteria in the low-nutrient surface waters of the subtropical ocean, but the basis for their coexistence has not been quantitatively demonstrated. Here, we combine in situ microcosm experiments and an ecological model to show that this coexistence can be sustained by specialization in the uptake of distinct nitrogen (N) substrates at low-level concentrations that prevail in subtropical environments. In field incubations, the response of both Prochlorococcus and Synechococcus to nanomolar N amendments demonstrates N limitation of growth in both populations. However, Prochlorococcus showed a higher affinity to ammonium, whereas Synechococcus was more adapted to nitrate uptake. A simple ecological model demonstrates that the differential nutrient preference inferred from field experiments with these genera may sustain their coexistence. It also predicts that as the supply of NO3- decreases, as expected under climate warming, the dominant genera should undergo a nonlinear shift from Synechococcus to Prochlorococcus, a pattern that is supported by subtropical field observations. Our study suggests that the evolution of differential nutrient affinities is an important mechanism for sustaining the coexistence of genera and that climate change is likely to shift the relative abundance of the dominant plankton genera in the largest biomes in the ocean. IMPORTANCE Our manuscript addresses the following fundamental question in microbial ecology: how do different plankton using the same essential nutrients coexist? Prochlorococcus and Synechococcus are the two dominant picocyanobacteria in the low-nutrient surface waters of the subtropical ocean, which support a significant amount of marine primary production. The geographical distributions of these two organisms are largely overlapping, but the basis for their coexistence in these biomes remains unclear. In this study, we combined in situ microcosm experiments and an ecosystem model to show that the coexistence of these two organisms can arise from specialization in the uptake of distinct nitrogen substrates; Prochlorococcus prefers ammonium, whereas Synechococcus prefers nitrate when these nutrients exist at low concentrations. Our framework can be used for simulating and predicting the coexistence in the future ocean and may provide hints toward understanding other similar types of coexistence.

Haptophyte communities along the Kuroshio current reveal their geographical sources and ecological traits.

Haptophytes are one of the most ecologically successful phytoplankton groups in the modern ocean and tend to maintain balanced and stable communities across various environments. However, little is known about the mechanisms that enable community stability and ecological success. To reveal the community characteristics and interactions among haptophytes, we conducted comprehensive observations from the upstream to downstream regions of the Kuroshio Current. Haptophyte abundance and taxonomy were assessed using quantitative polymerase chain reaction and metabarcoding of 18S rRNA sequences, respectively. The haptophyte community structure changed abruptly at sites on the shelf-slope of the East China Sea, indicating the strong influence of shelf waters with high phytoplankton biomass on downstream communities. Correlation network analysis combined with the phylogeny suggested that haptophytes can coexist with their close relatives, possibly owing to their nutritional flexibility, thereby escaping from resource competition. Consistently, some noncalcifying haptophyte genera with high mixotrophic capacities such as Chrysochromulina constituted a major component of the co-occurrence network, whereas coccolithophores such as Emiliania/Gephyrocapsa were rarely observed. Our study findings suggest that noncalcifying haptophytes play crucial roles in community diversity and stability, and in sustaining the food web structure in the Kuroshio ecosystems.

Crocosphaera as a Major Consumer of Fixed Nitrogen.

Crocosphaera watsonii (hereafter referred to as Crocosphaera) is a key nitrogen (N) fixer in the ocean, but its ability to consume combined-N sources is still unclear. Using in situ microcosm incubations with an ecological model, we show that Crocosphaera has high competitive capability both under low and moderately high combined-N concentrations. In field incubations, Crocosphaera accounted for the highest consumption of ammonium and nitrate, followed by picoeukaryotes. The model analysis shows that cells have a high ammonium uptake rate (~7 mol N [mol N]-1 d-1 at the maximum), which allows them to compete against picoeukaryotes and nondiazotrophic cyanobacteria when combined N is sufficiently available. Even when combined N is depleted, their capability of nitrogen fixation allows higher growth rates compared to potential competitors. These results suggest the high fitness of Crocosphaera in combined-N limiting, oligotrophic oceans heightening its potential significance in its ecosystem and in biogeochemical cycling. IMPORTANCE Crocosphaera watsonii is as a key nitrogen (N) supplier in marine ecosystems, and it has been estimated to contribute up to half of oceanic N2 fixation. Conversely, a recent study reported that Crocosphaera can assimilate combined N and proposed that unicellular diazotrophs can be competitors with non-N2 fixing phytoplankton for combined N. Despite its importance in nitrogen cycling, the methods by which Crocosphaera compete are not currently fully understood. Here, we present a new role of Crocosphaera as a combined-N consumer: a competitor against nondiazotrophic phytoplankton for combined N. In this study, we combined in situ microcosm experiments and an ecosystem model to quantitatively evaluate the combined-N consumption by Crocosphaera and other non-N2 fixing phytoplankton. Our results suggest the high fitness of Crocosphaera in combined-N limiting, oligotrophic oceans and, thus, heightens its potential significance in its ecosystem and in biogeochemical cycling.

Evaluation of origin-depended nitrogen input through atmospheric deposition and its effect on primary production in coastal areas of western Kyusyu, Japan.

Long term monitoring of atmospheric wet and dry depositions and associated nutrients fluxes was conducted on the coast of Japan facing the East China Sea continuously for 1 year and 2 months, with the origin of air mass investigated based on isotope analyses (Sr, Nd, and NO3). During the same period, intensive observations of ocean conditions and the chemical composition of sinking particles collected using sediment traps were conducted to investigate the effects of atmospheric deposition-derived nutrients on phytoplankton blooms. Dry-deposition-derived nutrient inputs to the surface ocean were larger during autumn to spring than in summer due to the effect of continental air mass occasionally carrying Asian dust (yellow sand). However, these nutrients fluxes were limited (1.1-1.5 mg-N m-2 day-1 on average) and didn't appear to cause phytoplankton blooms through the year. Although average dissolved inorganic nitrogen (DIN) concentrations in rainwater were lower in oceanic air masses compared to continental air masses, wet-deposition-derived nutrient inputs to the surface ocean on rainy days during the summer (26.0 mg-N m-2 day-1 on average) were large due to higher precipitation from oceanic air masses. Wet-deposition-derived nutrients significantly increased nutrient concentrations in the surface ocean and seemed to cause phytoplankton blooms in the warm rainy season when nutrients in the surface were depleted due to increased stratification. The increase in phytoplankton biomass was reflected in increased particle sinking into the bottom layer, as well as changing chemical characteristics. The supply of flesh phytoplankton-derived labile organic matter into the bottom layer could be expected to promote rapid bacterial decomposition and contribute to the formation of hypoxic water masses in early summer when the ocean was strongly stratified. Atmospheric deposition-derived nutrients in East Asia will have important impacts on not only the oligotrophic outer ocean but also surrounding coastal areas in the warm rainy season.

Nitrogen burden from atmospheric deposition in East Asian oceans in 2010 based on high-resolution regional numerical modeling.

East Asian oceans are possibly affected by a high nitrogen (N) burden because of the intense anthropogenic emissions in this region. Based on high-resolution regional chemical transport modeling with horizontal grid scales of 36 and 12 km, we investigated the N burden into East Asian oceans via atmospheric deposition in 2010. We found a high N burden of 2-9 kg N ha-1 yr-1 over the Yellow Sea, East China Sea (ECS), and Sea of Japan. Emissions over East Asia were dominated by ammonia (NH3) over land and nitrogen oxides (NOx) over oceans, and N deposition was dominated by reduced N over most land and open ocean, whereas it was dominated by oxidized N over marginal seas and desert areas. The verified numerical modeling identified that the following processes were quantitatively important over East Asian oceans: the dry deposition of nitric acid (HNO3), NH3, and coarse-mode (aerodynamic diameter greater than 2.5 µm) NO3-, and wet deposition of fine-mode (aerodynamic diameter less than 2.5 µm) NO3- and NH4+. The relative importance of the dry deposition of coarse-mode NO3- was higher over open ocean. The estimated N deposition to the whole ECS was 390 Gg N yr-1; this is comparable to the discharge from the Yangtze River to the ECS, indicating the significant contribution of atmospheric deposition. Based on the high-resolution modeling over the ECS, a tendency of high deposition in the western ECS and low deposition in the eastern ECS was found, and a variety of deposition processes were estimated. The dry deposition of coarse-mode NO3- and wet deposition of fine-mode NH4+ were the main factors, and the wet deposition of fine-mode NO3- over the northeastern ECS and wet deposition of coarse-mode NO3- over the southeastern ECS were also found to be significant processes determining N deposition over the ECS.

Distinct profiles of size-fractionated iron-binding ligands between the eastern and western subarctic Pacific.

Iron (Fe) is well known as a limiting factor to control primary productivity especially in high-nutrient and low chlorophyll area such as the subarctic Pacific. The solubility of Fe is believed to be controlled by its complexation with natural organic ligands, while the distribution of organic ligands is poorly understood. Here, we report that dissolved (< 0.2 µm) organic ligands were unevenly distributed between the western and eastern stations in the subarctic Pacific. The concentration of dissolved organic ligands around the lower part of subarctic Pacific intermediate water was higher in the western station, suggesting that Fe complexation with these organic ligands supports a lateral transport within the water mass. However, a more detailed size-fractionated treatment indicated no significant difference in the soluble (< 1000 kDa) ligands' distribution between the western and eastern stations. These results suggest that organic and inorganic colloid formations are potentially essential for Fe transport mechanisms in the subarctic Pacific.

Subpolar marginal seas fuel the North Pacific through the intermediate water at the termination of the global ocean circulation.

The mechanism by which nutrients in the deep ocean are uplifted to maintain nutrient-rich surface waters in the subarctic Pacific has not been properly described. The iron (Fe) supply processes that control biological production in the nutrient-rich waters are also still under debate. Here, we report the processes that determine the chemical properties of intermediate water and the uplift of Fe and nutrients to the main thermocline, which eventually maintains surface biological productivity. Extremely nutrient-rich water is pooled in intermediate water (26.8 to 27.6 σθ) in the western subarctic area, especially in the Bering Sea basin. Increases of two to four orders in the upward turbulent fluxes of nutrients were observed around the marginal sea island chains, indicating that nutrients are uplifted to the surface and are returned to the subarctic intermediate nutrient pool as sinking particles through the biological production and microbial degradation of organic substances. This nutrient circulation coupled with the dissolved Fe in upper-intermediate water (26.6 to 27.0 σθ) derived from the Okhotsk Sea evidently constructs an area that has one of the largest biological CO2 drawdowns in the world ocean. These results highlight the pivotal roles of the marginal seas and the formation of intermediate water at the end of the ocean conveyor belt.

Widespread Distribution and Expression of Gamma A (UMB), an Uncultured, Diazotrophic, γ-Proteobacterial nifH Phylotype.

Marine dinitrogen (N2) fixation studies have focused nearly exclusively on cyanobacterial diazotrophs; however γ-proteobacteria are an abundant component of the marine community and have been largely overlooked until recently. Here we present a phylogenetic analysis of all nifH γ-proteobacterial sequences available in public databases and qPCR data of a γ-proteobacterial phylotype, Gamma A (UMB), obtained during several research cruises. Our analysis revealed a complex diversity of diazotrophic γ-proteobacteria. One phylotype in particular, Gamma A, was described in several traditional and quantitative PCR studies. Though several γ-proteobacterial nifH sequences have been described as laboratory contaminants, Gamma A is part of a large cluster of sequences isolated from marine environments and distantly related to the clade of contaminants. Using a TaqMan probe and primer set, Gamma A nifH DNA abundance and expression were analyzed in nearly 1000 samples collected during 15 cruises to the Atlantic and Pacific Oceans. The data showed that Gamma A is an active, cosmopolitan diazotroph found throughout oxygenated, oligotrophic waters reaching maximum abundances of 8 x 104 nifH DNA copies l-1 and 5 x 105 nifH transcript copies l-1. Gamma A nifH transcript abundances were on average 3 fold higher than nifH DNA abundances. The widespread distribution and activity of Gamma A indicate that it has potential to be a globally important N2 fixing organism.

Equilibrator inlet-proton transfer reaction-mass spectrometry (EI-PTR-MS) for sensitive, high-resolution measurement of dimethyl sulfide dissolved in seawater.

We developed an equilibrator inlet-proton transfer reaction-mass spectrometry (EI-PTR-MS) method for fast detection of dimethyl sulfide (DMS) dissolved in seawater. Dissolved DMS extracted by bubbling pure nitrogen through the sample was continuously directed to the PTR-MS instrument. The equilibration of DMS between seawater and the carrier gas, and the response time of the system, were evaluated in the laboratory. DMS reached equilibrium with an overall response time of 1 min. The detection limit (50 pmol L(-1) at 5 s integration) was sufficient for detection of DMS concentrations in the open ocean. The EI-PTR-MS instrument was deployed during a research cruise in the western North Pacific Ocean. Comparison of the EI-PTR-MS results with results obtained by means of membrane tube equilibrator-gas chromatography/mass spectrometry agreed reasonably well on average (R(2) = 0.99). EI-PTR-MS captured temporal variations of dissolved DMS concentrations, including elevated peaks associated with patches of high biogenic activity. These results demonstrate that the EI-PTR-MS technique was effective for highly time-resolved measurements of DMS in the open ocean. Further measurements will improve our understanding of the biogeochemical mechanisms of the production, consumption, and distribution of DMS on the ocean surface and, hence, the air-sea flux of DMS, which is a climatically important species.

The decline and fate of an iron-induced subarctic phytoplankton bloom.

Iron supply has a key role in stimulating phytoplankton blooms in high-nitrate low-chlorophyll oceanic waters. However, the fate of the carbon fixed by these blooms, and how efficiently it is exported into the ocean's interior, remains largely unknown. Here we report on the decline and fate of an iron-stimulated diatom bloom in the Gulf of Alaska. The bloom terminated on day 18, following the depletion of iron and then silicic acid, after which mixed-layer particulate organic carbon (POC) concentrations declined over six days. Increased particulate silica export via sinking diatoms was recorded in sediment traps at depths between 50 and 125 m from day 21, yet increased POC export was not evident until day 24. Only a small proportion of the mixed-layer POC was intercepted by the traps, with more than half of the mixed-layer POC deficit attributable to bacterial remineralization and mesozooplankton grazing. The depletion of silicic acid and the inefficient transfer of iron-increased POC below the permanent thermocline have major implications both for the biogeochemical interpretation of times of greater iron supply in the geological past, and also for proposed geo-engineering schemes to increase oceanic carbon sequestration.

A mesoscale iron enrichment in the western subarctic Pacific induces a large centric diatom bloom.

We have performed an in situ test of the iron limitation hypothesis in the subarctic North Pacific Ocean. A single enrichment of dissolved iron caused a large increase in phytoplankton standing stock and decreases in macronutrients and dissolved carbon dioxide. The dominant phytoplankton species shifted after the iron addition from pennate diatoms to a centric diatom, Chaetoceros debilis, that showed a very high growth rate, 2.6 doublings per day. We conclude that the bioavailability of iron regulates the magnitude of the phytoplankton biomass and the key phytoplankton species that determine the biogeochemical sensitivity to iron supply of high-nitrate, low-chlorophyll waters.