Authigenic mineral phases as a driver of the upper-ocean iron cycle.

Iron is important in regulating the ocean carbon cycle1. Although several dissolved and particulate species participate in oceanic iron cycling, current understanding emphasizes the importance of complexation by organic ligands in stabilizing oceanic dissolved iron concentrations2-6. However, it is difficult to reconcile this view of ligands as a primary control on dissolved iron cycling with the observed size partitioning of dissolved iron species, inefficient dissolved iron regeneration at depth or the potential importance of authigenic iron phases in particulate iron observational datasets7-12. Here we present a new dissolved iron, ligand and particulate iron seasonal dataset from the Bermuda Atlantic Time-series Study (BATS) region. We find that upper-ocean dissolved iron dynamics were decoupled from those of ligands, which necessitates a process by which dissolved iron escapes ligand stabilization to generate a reservoir of authigenic iron particles that settle to depth. When this 'colloidal shunt' mechanism was implemented in a global-scale biogeochemical model, it reproduced both seasonal iron-cycle dynamics observations and independent global datasets when previous models failed13-15. Overall, we argue that the turnover of authigenic particulate iron phases must be considered alongside biological activity and ligands in controlling ocean-dissolved iron distributions and the coupling between dissolved and particulate iron pools.

Transport-limited reactions in microbial systems.

Predicting microbial metabolic rates and emergent biogeochemical fluxes remains challenging due to the many unknown population dynamical, physiological and reaction-kinetic parameters and uncertainties in species composition. Here, we show that the need for these parameters can be eliminated when population dynamics and reaction kinetics operate at much shorter time scales than physical mixing processes. Such scenarios are widespread in poorly mixed water columns and sediments. In this 'fast-reaction-transport' (FRT) limit, all that is required for predictions are chemical boundary conditions, the physical mixing processes and reaction stoichiometries, while no knowledge of species composition, physiology or population/reaction kinetic parameters is needed. Using time-series data spanning years 2001-2014 and depths 180-900 m across the permanently anoxic Cariaco Basin, we demonstrate that the FRT approach can accurately predict the dynamics of major electron donors and acceptors (Pearson r ≥ 0.9 in all cases). Hence, many microbial processes in this system are largely transport limited and thus predictable regardless of species composition, population dynamics and kinetics. Our approach enables predictions for many systems in which microbial community dynamics and kinetics are unknown. Our findings also reveal a mechanism for the frequently observed decoupling between function and taxonomy in microbial systems.

The integral role of iron in ocean biogeochemistry.

The micronutrient iron is now recognized to be important in regulating the magnitude and dynamics of ocean primary productivity, making it an integral component of the ocean's biogeochemical cycles. In this Review, we discuss how a recent increase in observational data for this trace metal has challenged the prevailing view of the ocean iron cycle. Instead of focusing on dust as the major iron source and emphasizing iron's tight biogeochemical coupling to major nutrients, a more complex and diverse picture of the sources of iron, its cycling processes and intricate linkages with the ocean carbon and nitrogen cycles has emerged.

Pervasive iron limitation at subsurface chlorophyll maxima of the California Current.

Subsurface chlorophyll maximum layers (SCMLs) are nearly ubiquitous in stratified water columns and exist at horizontal scales ranging from the submesoscale to the extent of oligotrophic gyres. These layers of heightened chlorophyll and/or phytoplankton concentrations are generally thought to be a consequence of a balance between light energy from above and a limiting nutrient flux from below, typically nitrate (NO3). Here we present multiple lines of evidence demonstrating that iron (Fe) limits or with light colimits phytoplankton communities in SCMLs along a primary productivity gradient from coastal to oligotrophic offshore waters in the southern California Current ecosystem. SCML phytoplankton responded markedly to added Fe or Fe/light in experimental incubations and transcripts of diatom and picoeukaryote Fe stress genes were strikingly abundant in SCML metatranscriptomes. Using a biogeochemical proxy with data from a 40-y time series, we find that diatoms growing in California Current SCMLs are persistently Fe deficient during the spring and summer growing season. We also find that the spatial extent of Fe deficiency within California Current SCMLs has significantly increased over the last 25 y in line with a regional climate index. Finally, we show that diatom Fe deficiency may be common in the subsurface of major upwelling zones worldwide. Our results have important implications for our understanding of the biogeochemical consequences of marine SCML formation and maintenance.

Synechococcus nitrogen gene loss in iron-limited ocean regions.

Synechococcus are the most abundant cyanobacteria in high latitude regions and are responsible for an estimated 17% of annual marine net primary productivity. Despite their biogeochemical importance, Synechococcus populations have been unevenly sampled across the ocean, with most studies focused on low-latitude strains. In particular, the near absence of Synechococcus genomes from high-latitude, High Nutrient Low Chlorophyll (HNLC) regions leaves a gap in our knowledge of picocyanobacterial adaptations to iron limitation and their influence on carbon, nitrogen, and iron cycles. We examined Synechococcus populations from the subarctic North Pacific, a well-characterized HNLC region, with quantitative metagenomics. Assembly with short and long reads produced two near complete Synechococcus metagenome-assembled genomes (MAGs). Quantitative metagenome-derived abundances of these populations matched well with flow cytometry counts, and the Synechococcus MAGs were estimated to comprise >99% of the Synechococcus at Station P. Whereas the Station P Synechococcus MAGs contained multiple genes for adaptation to iron limitation, both genomes lacked genes for uptake and assimilation of nitrate and nitrite, suggesting a dependence on ammonium, urea, and other forms of recycled nitrogen leading to reduced iron requirements. A global analysis of Synechococcus nitrate reductase abundance in the TARA Oceans dataset found nitrate assimilation genes are also lower in other HNLC regions. We propose that nitrate and nitrite assimilation gene loss in Synechococcus may represent an adaptation to severe iron limitation in high-latitude regions where ammonium availability is higher. Our findings have implications for models that quantify the contribution of cyanobacteria to primary production and subsequent carbon export.

Insights into the bioavailability of oceanic dissolved Fe from phytoplankton uptake kinetics.

Phytoplankton growth in large parts of the world ocean is limited by low availability of dissolved iron (dFe), restricting oceanic uptake of atmospheric CO2. The bioavailability of dFe in seawater is however difficult to appraise since it is bound by a variety of poorly characterized organic ligands. Here, we propose a new approach for evaluating seawater dFe bioavailability based on its uptake rate constant by Fe-limited cultured phytoplankton. We utilized seven phytoplankton species of diverse classes, sizes, and provenances to probe for dFe bioavailability in 12 seawater samples from several ocean basins and depths. All tested phytoplankton acquired organically bound Fe in any given sample at similar rates (after normalizing to cellular surface area), confirming that multiple, Fe-limited phytoplankton species can be used to probe dFe bioavailability in seawater. These phytoplankton-based uptake rate constants allowed us to compare water types, and obtain a grand average estimate of seawater dFe bioavailability. Among water types, dFe bioavailability varied by approximately four-fold, and did not clearly correlate with Fe concentrations or any of the measured Fe speciation parameters. Compared with well-studied Fe complexes, seawater dFe is more available than model siderophore Fe, but less available than inorganic Fe. Exposure of seawater to sunlight, however, significantly enhanced dFe bioavailability. The rate constants established in this work, not only facilitate comparison between water types, but also allow calculation of Fe uptake rates by phytoplankton in the ocean based on measured dFe concentrations. The approach established and verified in this study, opens a new way for determining dFe bioavailability in samples across the ocean, and enables modeling of in situ Fe uptake rates by phytoplankton using dFe concentrations from GEOTRACES datasets.

Corrigendum: Meta-omic signatures of microbial metal and nitrogen cycling in marine oxygen minimum zones.

[This corrects the article DOI: 10.3389/fmicb.2015.00998.].

Effect of marine antifouling paint particles waste on survival of natural Bermuda copepod communities.

Marine antifouling paints (MAPs) are widely used to prevent organisms from fouling vessel hulls. When scraped from vessels as part of regular maintenance, MAP particles discharged into the seawater become a source of toxic substances, like copper (Cu), to the environment, and biocides leaching from them are known to cause toxic effects on non-target organisms. We investigated the toxicity of MAP particles collected from a Bermuda boatyard on local copepod communities using two experiments. Copepod survival, Chlorophyll a and total dissolved Cu concentrations were measured before and after MAP particles addition. In an acute toxicity test, the addition of 0.3 g/L of MAP particles resulted in 0% copepods survival within 88 h and increased dissolved Cu by 1.8 µM. A significant inverse relationship was observed between copepod survival and MAP particles quantity, highlighting the toxic effects of MAP particles from boat maintenance on copepod communities in the surrounding seawater.

The Scientific Legacy of the CARIACO Ocean Time-Series Program.

The CARIACO (Carbon Retention in a Colored Ocean) Ocean Time-Series Program station, located at 10.50°N, 64.66°W, observed biogeochemical and ecological processes in the Cariaco Basin of the southwestern Caribbean Sea from November 1995 to January 2017. The program completed 232 monthly core cruises, 40 sediment trap deployment cruises, and 40 microbiogeochemical process cruises. Upwelling along the southern Caribbean Sea occurs from approximately November to August. High biological productivity (320-628 g C m-2 y-1) leads to large vertical fluxes of particulate organic matter, but only approximately 9-10 g C m-2 y-1 fall to the bottom sediments (∼1-3% of primary production). A diverse community of heterotrophic and chemoautotrophic microorganisms, viruses, and protozoa thrives within the oxic-anoxic interface. A decrease in upwelling intensity from approximately 2003 to 2013 and the simultaneous overfishing of sardines in the region led to diminished phytoplankton bloom intensities, increased phytoplankton diversity, and increased zooplankton densities. The deepest waters of the Cariaco Basin exhibited long-term positive trends in temperature, salinity, hydrogen sulfide, ammonia, phosphate, methane, and silica. Earthquakes and coastal flooding also resulted in the delivery of sediment to the seafloor. The program's legacy includes climate-quality data from suboxic and anoxic habitats and lasting relationships between international researchers.

Meta-omic signatures of microbial metal and nitrogen cycling in marine oxygen minimum zones.

Iron (Fe) and copper (Cu) are essential cofactors for microbial metalloenzymes, but little is known about the metalloenyzme inventory of anaerobic marine microbial communities despite their importance to the nitrogen cycle. We compared dissolved O2, NO[Formula: see text], NO[Formula: see text], Fe and Cu concentrations with nucleic acid sequences encoding Fe and Cu-binding proteins in 21 metagenomes and 9 metatranscriptomes from Eastern Tropical North and South Pacific oxygen minimum zones and 7 metagenomes from the Bermuda Atlantic Time-series Station. Dissolved Fe concentrations increased sharply at upper oxic-anoxic transition zones, with the highest Fe:Cu molar ratio (1.8) occurring at the anoxic core of the Eastern Tropical North Pacific oxygen minimum zone and matching the predicted maximum ratio based on data from diverse ocean sites. The relative abundance of genes encoding Fe-binding proteins was negatively correlated with O2, driven by significant increases in genes encoding Fe-proteins involved in dissimilatory nitrogen metabolisms under anoxia. Transcripts encoding cytochrome c oxidase, the Fe- and Cu-containing terminal reductase in aerobic respiration, were positively correlated with O2 content. A comparison of the taxonomy of genes encoding Fe- and Cu-binding vs. bulk proteins in OMZs revealed that Planctomycetes represented a higher percentage of Fe genes while Thaumarchaeota represented a higher percentage of Cu genes, particularly at oxyclines. These results are broadly consistent with higher relative abundance of genes encoding Fe-proteins in the genome of a marine planctomycete vs. higher relative abundance of genes encoding Cu-proteins in the genome of a marine thaumarchaeote. These findings highlight the importance of metalloenzymes for microbial processes in oxygen minimum zones and suggest preferential Cu use in oxic habitats with Cu > Fe vs. preferential Fe use in anoxic niches with Fe > Cu.

The organic complexation of iron in the marine environment: a review.

Iron (Fe) is an essential micronutrient for marine organisms, and it is now well established that low Fe availability controls phytoplankton productivity, community structure, and ecosystem functioning in vast regions of the global ocean. The biogeochemical cycle of Fe involves complex interactions between lithogenic inputs (atmospheric, continental, or hydrothermal), dissolution, precipitation, scavenging, biological uptake, remineralization, and sedimentation processes. Each of these aspects of Fe biogeochemical cycling is likely influenced by organic Fe-binding ligands, which complex more than 99% of dissolved Fe. In this review we consider recent advances in our knowledge of Fe complexation in the marine environment and their implications for the biogeochemistry of Fe in the ocean. We also highlight the importance of constraining the dissolved Fe concentration value used in interpreting voltammetric titration data for the determination of Fe speciation. Within the published Fe speciation data, there appear to be important temporal and spatial variations in Fe-binding ligand concentrations and their conditional stability constants in the marine environment. Excess ligand concentrations, particularly in the truly soluble size fraction, seem to be consistently higher in the upper water column, and especially in Fe-limited, but productive, waters. Evidence is accumulating for an association of Fe with both small, well-defined ligands, such as siderophores, as well as with larger, macromolecular complexes like humic substances, exopolymeric substances, and transparent exopolymers. The diverse size spectrum and chemical nature of Fe ligand complexes corresponds to a change in kinetic inertness which will have a consequent impact on biological availability. However, much work is still to be done in coupling voltammetry, mass spectrometry techniques, and process studies to better characterize the nature and cycling of Fe-binding ligands in the marine environment.

Phytoplankton responses to atmospheric metal deposition in the coastal and open-ocean Sargasso Sea.

This study investigated the impact of atmospheric metal deposition on natural phytoplankton communities at open-ocean and coastal sites in the Sargasso Sea during the spring bloom. Locally collected aerosols with different metal contents were added to natural phytoplankton assemblages from each site, and changes in nitrate, dissolved metal concentration, and phytoplankton abundance and carbon content were monitored. Addition of aerosol doubled the concentrations of cadmium (Cd), cobalt (Co), copper (Cu), iron (Fe), manganese (Mn), and nickel (Ni) in the incubation water. Over the 3-day experiments, greater drawdown of dissolved metals occurred in the open ocean water, whereas little metal drawdown occurred in the coastal water. Two populations of picoeukaryotic algae and Synechococcus grew in response to aerosol additions in both experiments. Particulate organic carbon increased and was most sensitive to changes in picoeukaryote abundance. Phytoplankton community composition differed depending on the chemistry of the aerosol added. Enrichment with aerosol that had higher metal content led to a 10-fold increase in Synechococcus abundance in the oceanic experiment but not in the coastal experiment. Enrichment of aerosol-derived Co, Mn, and Ni were particularly enhanced in the oceanic experiment, suggesting the Synechococcus population may have been fertilized by these aerosol metals. Cu-binding ligand concentrations were in excess of dissolved Cu in both experiments, and increased with aerosol additions. Bioavailable free hydrated Cu(2+) concentrations were below toxicity thresholds throughout both experiments. These experiments show (1) atmospheric deposition contributes biologically important metals to seawater, (2) these metals are consumed over time scales commensurate with cell growth, and (3) growth responses can differ between distinct Synechococcus or eukaryotic algal populations despite their relatively close geographic proximity and taxonomic similarity.

A review of total dissolved copper and its chemical speciation in San Francisco Bay, California.

Following basin-wide contamination from industrial emissions and urban development, total dissolved copper concentrations in some regions of San Francisco Bay have exceeded national and state guidelines for water quality. In the face of dramatic improvements in wastewater treatment and point source control, persisting elevated dissolved copper concentrations in the Bay have prompted multiple studies and extensive monitoring of this estuary since 1989. Statistical analyses of monitoring data show that total dissolved copper concentrations have declined in the North (by 17%) and South (29%) San Francisco Bay as well as in the Southern Sloughs (44%) from 1993 to 2001. Concentrations remain elevated in the farthest reaches of the Bay (Delta and Estuary Interface), and in the Central Bay. Dissolved copper concentrations throughout the Bay have also been positively correlated (r = 0.632, P < 0.0005, n = 598) with dissolved organic matter, supporting results from complimentary chemical speciation studies which indicate that high-affinity copper-binding organic ligands dominate the chemical speciation of dissolved copper in the Bay. These organic ligands typically bind > 99.9% of the dissolved copper, effectively buffering the system against small changes in dissolved copper concentrations, and maintaining free Cu(2+) concentrations well below the toxicity threshold of ambient aquatic microorganisms. In response to these findings, site-specific water quality criteria for dissolved copper concentrations are now being developed by the Regional Water Quality Board to provide a more appropriate standard for copper toxicity in the Bay-one based on its chemical speciation and bioavailability.