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Glacial meltwater from the western Antarctic Ice Sheet is hypothesized to be an important source of cryospheric iron, fertilizing the Southern Ocean, yet its trace-metal composition and factors that control its dispersal remain poorly constrained. Here we characterize meltwater iron sources in a heavily glaciated western Antarctic Peninsula (WAP) fjord. Using dissolved and particulate ratios of manganese to iron in meltwaters, porewaters, and seawater, we show that surface glacial melt and subglacial plumes contribute to the seasonal cycle of iron and manganese within a fjord still relatively unaffected by climate-change-induced glacial retreat. Organic ligands derived from the phytoplankton bloom and the glaciers bind dissolved iron and facilitate the solubilization of particulate iron downstream. Using a numerical model, we show that buoyant plumes generated by outflow from the subglacial hydrologic system, enriched in labile particulate trace metals derived from a chemically modified crustal source, can supply iron to the fjord euphotic zone through vertical mixing. We also show that prolonged katabatic wind events enhance export of meltwater out of the fjord. Thus, we identify an important atmosphere–ice–ocean coupling intimately tied to coastal iron biogeochemistry and primary productivity along the WAP.

Glacial meltwater from the western Antarctic Ice Sheet is hypothesized to be an important source of cryospheric iron, fertilizing the Southern Ocean, yet its trace metal composition and factors which control its dispersal remain poorly constrained. Here we characterize meltwater iron sources in a heavily glaciated western Antarctic Peninsula (WAP) fjord. Using dissolved and particulate ratios of manganese-to-iron in meltwaters, porewaters, and seawater, we show that glacial melt and subglacial plumes contribute to the seasonal cycle of bioavailable iron within a fjord still relatively unaffected by climate change-induced glacial retreat. Organic ligands derived from the phytoplankton bloom and the glaciers bind dissolved iron and facilitate the solubilization of particulate iron downstream. Using a numerical model, we show that plumes generated by outflow from the subglacial hydrologic system, enriched in labile particulate trace metals derived from a chemically-modified crustal source, can supply the surface through vertical mixing, and that prolonged katabatic wind events enhance export of meltwater out of the fjord. Thus, we identify an important atmosphere-ice-ocean coupling intimately tied to coastal iron biogeochemistry and primary productivity along the WAP.

Significance The vertical distribution of phytoplankton cells and chlorophyll concentrations throughout the sunlit water column is rarely uniform. In many ocean regions, chlorophyll concentrations peak in distinct and persistent layers deep below the surface called subsurface chlorophyll maximum layers (SCMLs). SCML formation is hypothesized to reflect the consequences of phytoplankton light/macronutrient colimitation, behavior, and/or photoacclimation. We discovered unexpectedly persistent and widespread phytoplankton iron limitation and iron/light colimitation in SCMLs of the California Current and at the edge of the North Pacific Subtropical Gyre using shipboard incubations, metatranscriptomics, and biogeochemical proxies. These results suggest that interactions and feedbacks between iron and light availability play an important and previously unrecognized role in controlling the productivity and biogeochemical dynamics of SCMLs., 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.

It is now widely accepted that siderophores play a role in marine iron biogeochemical cycling. However, the mechanisms by which siderophores affect the availability of iron from specific sources and the resulting significance of these processes on iron biogeochemical cycling as a whole have remained largely untested. In this study, we develop a model system for testing the effects of siderophore production on iron bioavailability using the marine copiotroph Alteromonas macleodii ATCC 27126. Through the generation of the knockout cell line ΔasbB::kmr, which lacks siderophore biosynthetic capabilities, we demonstrate that the production of the siderophore petrobactin enables the acquisition of iron from mineral sources and weaker iron-ligand complexes. Notably, the utilization of lithogenic iron, such as that from atmospheric dust, indicates a significant role for siderophores in the incorporation of new iron into marine systems. We have also detected petrobactin, a photoreactive siderophore, directly from seawater in the mid-latitudes of the North Pacific and have identified the biosynthetic pathway for petrobactin in bacterial metagenome-assembled genomes widely distributed across the global ocean. Together, these results improve our mechanistic understanding of the role of siderophore production in iron biogeochemical cycling in the marine environment wherein iron speciation, bioavailability, and residence time can be directly influenced by microbial activities.

As the major facilitators of the turnover of organic matter in the marine environment, the ability of heterotrophic bacteria to acquire specific compounds within the diverse range of dissolved organic matter will affect the regeneration of essential nutrients such as iron and carbon. TonB-dependent transporters are a prevalent cellular tool in Gram-negative bacteria that allow a relatively high-molecular-weight fraction of organic matter to be directly accessed. However, these transporters are not well characterized in marine bacteria, limiting our understanding of the flow of specific substrates through the marine microbial loop. Here, we characterize the TonB-dependent transporters responsible for iron and carbon acquisition in a representative marine copiotroph and examine their distribution across the genus Alteromonas. We provide evidence that substrate-specific bioavailability is niche specific, particularly for iron complexes, indicating that transport capacity may serve as a significant control on microbial community dynamics and the resultant cycling of organic matter., Iron is an essential micronutrient for all microbial growth in the marine environment, and in heterotrophic bacteria, iron is tightly linked to carbon metabolism due to its central role as a cofactor in enzymes of the respiratory chain. Here, we present the iron- and carbon-regulated transcriptomes of a representative marine copiotroph, Alteromonas macleodii ATCC 27126, and characterize its cellular transport mechanisms. ATCC 27126 has distinct metabolic responses to iron and carbon limitation and, accordingly, uses distinct sets of TonB-dependent transporters for the acquisition of iron and carbon. These distinct sets of TonB-dependent transporters were of a similar number, indicating that the diversity of carbon and iron substrates available to ATCC 27126 is of a similar scale. For the first time in a marine bacterium, we have also identified six characteristic inner membrane permeases for the transport of siderophores via an ATPase-independent mechanism. An examination of the distribution of specific TonB-dependent transporters in 31 genomes across the genus Alteromonas points to niche specialization in transport capacity, particularly for iron. We conclude that the substrate-specific bioavailability of both iron and carbon in the marine environment will likely be a key control on the processing of organic matter through the microbial loop. IMPORTANCE As the major facilitators of the turnover of organic matter in the marine environment, the ability of heterotrophic bacteria to acquire specific compounds within the diverse range of dissolved organic matter will affect the regeneration of essential nutrients such as iron and carbon. TonB-dependent transporters are a prevalent cellular tool in Gram-negative bacteria that allow a relatively high-molecular-weight fraction of organic matter to be directly accessed. However, these transporters are not well characterized in marine bacteria, limiting our understanding of the flow of specific substrates through the marine microbial loop. Here, we characterize the TonB-dependent transporters responsible for iron and carbon acquisition in a representative marine copiotroph and examine their distribution across the genus Alteromonas. We provide evidence that substrate-specific bioavailability is niche specific, particularly for iron complexes, indicating that transport capacity may serve as a significant control on microbial community dynamics and the resultant cycling of organic matter.

In vast areas of the ocean, the scarcity of iron controls the growth and productivity of phytoplankton. Although most dissolved iron in the marine environment is complexed with organic molecules, picomolar amounts of labile inorganic iron species (labile iron) are maintained within the euphotic zone and serve as an important source of iron for eukaryotic phytoplankton and particularly for diatoms. Genome-enabled studies of labile iron utilization by diatoms have previously revealed novel iron-responsive transcripts, including the ferric iron-concentrating protein ISIP2A, but the mechanism behind the acquisition of picomolar labile iron remains unknown. Here we show that ISIP2A is a phytotransferrin that independently and convergently evolved carbonate ion-coordinated ferric iron binding. Deletion of ISIP2A disrupts high-affinity iron uptake in the diatom Phaeodactylum tricornutum, and uptake is restored by complementation with human transferrin. ISIP2A is internalized by endocytosis, and manipulation of the seawater carbonic acid system reveals a second-order dependence on the concentrations of labile iron and carbonate ions. In P. tricornutum, the synergistic interaction of labile iron and carbonate ions occurs at environmentally relevant concentrations, revealing that carbonate availability co-limits iron uptake. Phytotransferrin sequences have a broad taxonomic distribution and are abundant in marine environmental genomic datasets, suggesting that acidification-driven declines in the concentration of seawater carbonate ions will have a negative effect on this globally important eukaryotic iron acquisition mechanism.

Continental margins are an important external source of dissolved iron to the marine environment. However, the mechanisms responsible for the offshore transport of dissolved iron is impacted by the resulting iron speciation. We characterized the iron speciation in the Eastern Tropical North Pacific (ETNP) oxygen deficient zone (ODZ), including dissolved iron, organic iron-binding ligands, and reduced iron. Organic iron-binding ligands were measured using both competitive ligand exchange adsorptive cathodic stripping voltammetry (CLE-ACSV) and liquid chromatography electrospray ionization mass spectrometry (LC-ESI-MS) in order to explore the impact of organic ligands on dissolved iron (dFeT) and iron(II) biogeochemistry in the region. Organic ligands were present in high concentrations (1.06–5.30 nmol L−1) and exceeded dissolved iron concentrations (0.36–4.52 nmol L−1) at all locations. Iron-binding strengths ( log K FeL , Fe ′ cond ) ranged 11.22 to 12.75 and were elevated in the ODZ layer relative to the oxygenated water column. LC-ESI-MS revealed the presence of siderophores, or bacterially-produced organic ligands with high Fe-affinity, in all samples analyzed, suggesting these compounds may be produced by microbes in the ODZ despite high ambient dFeT concentrations. This study is the first to characterize siderophores in an ODZ environment to date, and the three siderophores found (amphibactin B, synechobactin c9, synechobactin c10) could contribute to the observed elevated log K FeL , Fe ′ cond of ligands in the ODZ. Comparative analysis of organic ligand log K FeL , Fe ′ cond values in other low oxygen environments suggests that strong ligands, including siderophores, could be present in other low oxygen regions. In a simple model of the shelf-to-offshore iron transport mechanism, strong organic iron-binding ligands had a large impact on the longevity and transport of iron in the ODZ. These results suggest that organic ligand composition can have an impact on iron distributions in the ETNP ODZ and regulate the offshore transport of iron to the open ocean.

Picocyanobacteria from the genus Synechococcus are ubiquitous in ocean waters. Their phylogenetic and genomic diversity suggests ecological niche differentiation, but the selective forces influencing this are not well defined. Marine picocyanobacteria are sensitive to Cu toxicity, so adaptations to this stress could represent a selective force within, and between, 'species', also known as clades. Here, we compared Cu stress responses in cultures and natural populations of marine Synechococcus from two co-occurring major mesotrophic clades (I and IV). Using custom microarrays and proteomics to characterize expression responses to Cu in the lab and field, we found evidence for a general stress regulon in marine Synechococcus. However, the two clades also exhibited distinct responses to copper. The Clade I representative induced expression of genomic island genes in cultures and Southern California Bight populations, while the Clade IV representative downregulated Fe-limitation proteins. Copper incubation experiments suggest that Clade IV populations may harbour stress-tolerant subgroups, and thus fitness tradeoffs may govern Cu-tolerant strain distributions. This work demonstrates that Synechococcus has distinct adaptive strategies to deal with Cu toxicity at both the clade and subclade level, implying that metal toxicity and stress response adaptations represent an important selective force for influencing diversity within marine Synechococcus populations.

Although marine bacteria were identified nearly two decades ago as potential sources for strong iron‐binding organic ligands detected in seawater, specific linkages between ligands detected in natural water and the microbial community remain unclear. We compared the production of different classes of iron‐binding ligands, dissolved iron and macronutrient concentrations, and phytoplankton and bacterioplankton assemblages in a series of iron amended 6‐d incubations. Incubations with high iron additions had near complete macronutrient consumption and higher phytoplankton biomass compared with incubations with low iron additions, but both iron treatments were dominated by diatoms. However, we only detected the strongest ligands in high‐iron treatments, and strong iron‐binding ligands were generally correlated with an increased abundance of copiotrophic bacteria, particularly Alteromonas strains. Ultimately, these robust correlations suggest a potential linkage between copiotrophic bacteria and strong iron‐binding ligand production after iron fertilization events in the marine environment.

Author(s): Stukel, MR; Kelly, TB; Aluwihare, LI; Barbeau, KA; Goericke, R; Krause, JW; Landry, MR; Ohman, MD | Abstract: We investigated variability in the C:234Th ratio of sinking particles and its relationship to changing water column characteristics and plankton ecological dynamics during 29 Lagrangian experiments conducted on six cruises of the California Current Ecosystem Long-Term Ecological Research (CCE-LTER) Program. C:234Th ratios of sinking particles collected by a surface-tethered sediment trap (C:234ThST) varied from 2.3 to 20.5 μmol C dpm−1 over a depth range of 47–150 m. C:234ThST was significantly greater (by a factor of 1.8) than C:234Th ratios of suspended g51-μm particles collected in the same water parcels with in situ pumps. C:234Th ratios of large (g200-μm) sinking particles also exceeded those of smaller sinking particles. C:234ThST decreased with depth from the base of the euphotic zone through the upper twilight zone. C:234ThST was positively correlated with several indices of ecosystem productivity including particulate organic carbon (POC) and chlorophyll (Chl) concentrations, mesozooplankton biomass, and the fraction of Chl g20-μm. Principal component analysis and multiple linear regression suggested that decaying phytoplankton blooms exhibited higher C:234ThST than actively growing blooms at similar biomass levels. C:234ThST was positively correlated with indices of the fractional contribution of fecal pellets in sediment traps when the proportion of fecal pellets was low in the traps, likely because of a correlation between mesozooplankton biomass and other indices of ecosystem productivity. However, when fecal pellets were a more important component of sinking material, C:234ThST decreased with increasing fecal pellet content. C:234ThST was also positively correlated with the Si:C ratio of sinking particles. Across the dataset (and across depths) a strong correlation was found between C:234ThST and the ratio of vertically-integrated POC to vertically-integrated total water column 234Th (vC:234Thtot). A mechanistic one-layer, two-box model of thorium sorption and desorption was invoked to explain this correlation. Two empirical models (one using vC:234Thtot; one using depth and vertically-integrated Chl) were developed to predict C:234Th ratios in this coastal upwelling biome. The former regression (log10(C:234ThST) = 0.43 × log10(vC:234Thtot) + 0.53) was found to also be a reasonable predictor for C:234ThST from diverse regions including the Southern Ocean, Sargasso Sea, Subarctic North Pacific, and Eastern Tropical North Pacific.

It is well recognized that the atmospheric deposition of iron (Fe) affects ocean productivity, atmospheric CO2 uptake, ecosystem diversity, and overall climate. Despite significant advances in measurement techniques and modeling efforts, discrepancies persist between observations and models that hinder accurate predictions of processes and their global effects. Here, we provide an assessment report on where the current state of knowledge is and where future research emphasis would have the highest impact in furthering the field of Fe atmosphere-ocean biogeochemical cycle. These results were determined through consensus reached by diverse researchers from the oceanographic and atmospheric science communities with backgrounds in laboratory and in situ measurements, modeling, and remote sensing. We discuss i) novel measurement methodologies and instrumentation that allow detection and speciation of different forms and oxidation states of Fe in deliquesced mineral aerosol, cloud/rainwater, and seawater; ii) oceanic models that treat Fe cycling with several external sources and sinks, dissolved, colloidal, particulate, inorganic, and organic ligand-complexed forms of Fe, as well as Fe in detritus and phytoplankton; and iii) atmospheric models that consider natural and anthropogenic sources of Fe, mobilization of Fe in mineral aerosols due to the dissolution of Fe-oxides and Fe-substituted aluminosilicates through proton-promoted, organic ligand-promoted, and photo-reductive mechanisms. In addition, the study identifies existing challenges and disconnects (both fundamental and methodological) such as i) inconsistencies in Fe nomenclature and the definition of bioavailable Fe between oceanic and atmospheric disciplines, and ii) the lack of characterization of the processes controlling Fe speciation and residence time at the atmosphere-ocean interface. Such challenges are undoubtedly caused by extremely low concentrations, short lifetime, and the myriad of physical, (photo)chemical, and biological processes affecting global biogeochemical cycling of Fe. However, we also argue that the historical division (separate treatment of Fe biogeochemistry in oceanic and atmospheric disciplines) and the classical funding structures (that often create obstacles for transdisciplinary collaboration) are also hampering the advancement of knowledge in the field. Finally, the study provides some specific ideas and guidelines for laboratory studies, field measurements, and modeling research required for improved characterization of global biogeochemical cycling of Fe in relationship with other trace elements and essential nutrients. The report is intended to aid scientists in their work related to Fe biogeochemistry as well as program managers at the relevant funding agencies.

Heterotrophic bacteria in the SAR11 and Roseobacter lineages shape the marine carbon, nitrogen, phosphorous, and sulfur cycles, yet they do so having adopted divergent ecological strategies. Currently, it is unknown whether these globally significant groups partition into specific niches with respect to micronutrients (e.g., trace metals) and how that may affect marine trace metal cycling. Here, we used comparative genomics to identify diverse iron, cobalt, nickel, copper, and zinc uptake capabilities in SAR11 and Roseobacter genomes and uncover surprising unevenness within and between lineages. The strongest predictors for the extent of the metal uptake gene content are the total number of transporters per genome, genome size, total metal transporters, and GC content, but numerous exceptions exist in both groups. Taken together, our results suggest that SAR11 have strongly minimized their trace metal uptake versatility, with high-affinity zinc uptake being a unique exception. The larger Roseobacter genomes have greater trace metal uptake versatility on average, but they also appear to have greater plasticity, resulting in phylogenetically similar genomes having largely different capabilities. Ultimately, phylogeny is predictive of the diversity and extent of 20 to 33% of all metal uptake systems, suggesting that specialization in metal utilization mostly occurred independently from overall lineage diversification in both SAR11 and Roseobacter . We interpret these results as reflecting relatively recent trace metal niche partitioning in both lineages, suggesting that concentrations and chemical forms of metals in the marine environment are important factors shaping the gene content of marine heterotrophic Alphaproteobacteria of the SAR11 and Roseobacter lineages.

In August 2010, iron (Fe) and Fe and copper (Cu) addition incubation experiments were conducted at two low Fe stations (P20 and P26) along Line P, off the western coast of British Columbia, to investigate Cu physiology in Fe- and Fe-light co-limited phytoplankton. Chlorophyll a concentrations ([Chl a]), maximum variable fluorescence yield (Fv/Fm), and Fe uptake rates by the Cu-dependent high-affinity Fe transport system (HAFeTS) were measured. Additions of Fe resulted in an increase in [Chl a] and Fv/Fm at both stations compared with the controls, regardless of light availability, and confirmed that the phytoplankton communities were Fe-limited. Uptake of Fe by the HAFeTS in both incubations increased with the addition of Fe, and likely reflects luxury Fe uptake and storage. While the in situ inorganic Cu concentrations were similar to those that can induce Cu-limitation in laboratory cultures, increasing Cu availability had no effect on biomass accumulation during both incubations, regardless of Fe availability or light regime. At P26, additions of 1 nmol L−1 CuSO4 resulted in a short-term increase in Fv/Fm of the phytoplankton community, and an increase in Fe uptake rates by large phytoplankton (>5 μm), but only when light was not limiting. These data confirm a complex interaction between light, Fe and Cu physiology in indigenous phytoplankton communities, and suggest that these interactions may be both spatially heterogeneous and different for different phytoplankton size classes.

Samples for organic copper (Cu)-binding ligand characterization were collected along the 2013 U.S. GEOTRACES Pacific (GP16) cruise transect from Peru to Tahiti. Full depth profiles of Cu speciation were collected across a dynamic range in oceanographic conditions including a highly productive coastal region, an oxygen deficient zone, a high nutrient low chlorophyll (HNLC) region, an oligotrophic region and a hydrothermal vent plume. Surface waters from Peru to Tahiti exhibited elevated dissolved Cu and ligand concentrations near Peru and then decreased in concentration (

The impact of ice-ocean interaction on the Southern Ocean is expected to intensify in the future. However, its influence on phytoplankton community composition remains an open question. The Antarctic Peninsula fjords offer an ideal system to understand the effect of ice-ocean forcing on phytoplankton community, providing an extreme in the spatial gradient from the glacio-marine boundary to the Western Antarctic Peninsula (WAP) continental shelf. During two cruises conducted in December 2015 and April 2016 in Andvord Bay, we found that glacial meltwater input altered surface salinity, promoting shallow mixed layers, and enriched surface waters in dissolved iron and nitrate. The three major groups of phytoplankton fueled by glacial input were: cryptophytes, diatoms, and a group of unidentified small flagellates. Prasinophytes and dinoflagellates were also present, in lower concentrations. In December, cryptophytes dominated the phytoplankton community and were correlated with relatively warmer temperatures in the surface layer; in addition, contrary to our hypothesis, no diatom bloom was observed in the fjord in spite of dissolved iron concentration >1 nM. By April, after the growth season, the overall phytoplankton abundance had decreased by an order of magnitude. Phytoplankton, in particular diatoms, were then limited by daytime length despite abundant macro-nutrient and iron concentrations. Mixed flagellates emerged as the dominant group during April due to the decline of other major taxa. Deep-learning algorithms for predicting the abundance of each major phytoplankton group captured the effects of these environmental factors on the phytoplankton community. Our results show that the fjord has relatively high phytoplankton biomass combined with high macro- and trace nutrient concentrations when compared to the broader WAP region. Based on this study, we confirm that flagellates can be the dominant taxon in Antarctic nearshore waters and we propose that iron concentration alone is insufficient to predict diatom growth. Furthermore, marine terminating glaciers in the WAP can enrich surface waters with nitrate even if the main fjord circulation is not driven by glacier meltwater discharge.

article Copper (Cu) is an essential micronutrient for marine phytoplankton, but can cause toxicity at elevated intracel- lular concentrations. The majority of Cu (N99.9%) in oceanic surface waters is bound to strong organic ligands, presumablyproduced byprokaryotestodetoxifyCu.Althoughlaboratory studieshave demonstratedthatorgan- ically complexed Cu may be bioavailable to marine eukaryotic phytoplankton, the bioavailability of Cu organic complexes to indigenous marine phytoplankton has not been examined in detail. Using the carrier free radioiso- tope 67 CuatanironlimitedstationinthenortheastsubarcticPacificOcean,weperformedsizefractionatedshort

Dissolved iron (dFe) and organic dFe-binding ligands were determined in San Francisco Bay, California by competitive ligand exchange adsorptive cathodic stripping voltammetry (CLE-ACSV) along a salinity gradient from the freshwater endmember of the Sacramento River (salinity 26). A range of dFe-binding ligand classes was simultaneously determined using multiple analytical window analysis, involving titrations with multiple concentrations of the added ligand, salicylaldoxime. The highest dFe and ligand concentrations were determined in the low salinity end of the estuary, with dFe equal to 131.5 nmol L− 1 and strong ligand (log K F e L , F e ′ cond ≥ 12.0) concentrations equal to 139.5 nmol L− 1. The weakest ligands (log K F e L , F e ′ cond K F e L , F e ′ cond > 11.0) were tightly coupled to dFe throughout the estuary, with average excess ligand concentrations ([L]–[dFe]) equal to 0.5 nmol L− 1. Humic-like substances analyzed via both CLE-ACSV and proton nuclear magnetic resonance in several samples were found to be a significant portion of the dFe-binding ligand pool in San Francisco Bay, with concentrations ranging from 559.5 μg L− 1 to 67.5 μg L− 1 in the lowest and highest salinity samples, respectively. DFe-binding ligands and humic-like substances were also found in benthic boundary layer samples taken from the shelf near the mouths of San Francisco Bay and Eel River, suggesting estuaries are an important source of dFe-binding ligands to California coastal shelf waters.

Nutrient dynamics, phytoplankton rate processes, and export were examined in a frontal region between an anticyclone and a pair of cyclones 120 km off the coast in the southern California Current System (sCCS). Low silicic acid: nitrate ratios (Si:N) and high nitrate to iron ratios (N:Fe) characteristic of Fe-limiting conditions in the sCCS were associated with the northern cyclone and with the transition zone between the cyclones and the anticyclone. Phytoplankton growth in low-Si:N, high-N:Fe waters responded strongly to added Fe, confirming growth limitation by Fe of the diatom-dominated phytoplankton community. Low Si:N waters had low biogenic silica content, intermediate productivity, but high export compared to intermediate Si:N waters indicating increased export efficiency under Fe stress. Biogenic silica and particulate organic carbon (POC) export were both high beneath low Si:N waters with biogenic silica export being especially enhanced. This suggests that relatively high POC export from low Si:N waters was supported by silica ballasting from Fe-limited diatoms. Higher POC export efficiency in low Si:N waters may have been further enhanced by lower rates of organic carbon remineralization due to reduced grazing of more heavily armored diatoms growing under Fe stress. The results imply that Fe stress can enhance carbon export, despite lowering productivity, by driving higher export efficiency.

The size partitioning of dissolved iron and organic iron-binding ligands into soluble and colloidal phases was investigated in the upper 150 m of two stations along the GA03 U.S. GEOTRACES North Atlantic transect. The size fractionation was completed using cross-flow filtration methods, followed by analysis by isotope dilution inductively-coupled plasma mass spectrometry (ID-ICP-MS) for iron and competitive ligand exchange-adsorptive cathodic stripping voltammetry (CLE-ACSV) for iron-binding ligands. On average, 80% of the 0.1–0.65 nM dissolved iron ( 99% of dissolved iron in the ocean is organically complexed. Disentangling the chemical form of iron in the upper ocean has important implications for surface ocean biogeochemistry and may affect iron uptake by phytoplankton.

With the common goal of more accurately and consistently quantifying ambient concentrations of free metal ions and natural organic ligands in aquatic ecosystems, researchers from 15 laboratories that routinely analyze trace metal speciation participated in an intercomparison of statistical methods used to model the most widely-obtained type of experimental dataset, the complexometric titration. All were asked to apply statistical techniques that they felt comfortable using to model synthetic titration curves that are typical of those obtained by applying state-of-the-art electrochemical methods – anodic stripping voltammetry (ASV) and competitive ligand equilibration/adsorptive cathodic stripping voltammetry (CLE-ACSV) – to the analysis of natural waters. Herein, we compare our estimates for parameters describing the natural ligands, examine the accuracy of inferred ambient free metal ion concentrations ([Mf]), and evaluate the influence of the various methods and assumptions used in analyzing the data on these results. The ASV- type titrations were designed to test each participants’ ability to correctly describe the natural ligands present in a sample when provided with data free of measurement error, i.e., random noise. For the three virtual samples containing just one natural ligand, all participants were able to correctly identify the number of ligand classes present and accurately estimate their parameter values. For the four virtual samples containing two or three ligand classes, a few participants detected too few or too many classes and consequently reported inaccurate “measurements” of ambient [Mf]. Since the problematic results arose from human error rather than any specific method of analyzing the data, we recommend that analysts should make a practice of using one’s parameter estimates to generate simulated (back-calculated) titration curves for comparison to the original data. The root-mean squared difference between the fitted observations and simulated curves should be comparable to the expected error of the analytical method and upon visual inspection the distribution of residuals should be unskewed. Modeling the synthetic, CLE-ACSV-type titration dataset proved to be more challenging. The participants were provided with five distinct titration curves generated at different levels of competing ligand added (analytical windows) to the virtual sample. Random measurement error was also incorporated. Comparison of the submitted results was complicated by the differing interpretations of our task. Most adopted the provided “true” instrumental sensitivity in modeling the CLE- ACSV curves, but several estimated sensitivities using internal calibration, exactly as is required for actual samples. Since the fitted sensitivities were biased low, systematic biases in inferred ambient [Mf] and in estimated weak ligand (L2) concentrations resulted from their use. The main distinction between the mathematical approaches taken by participants lies in their choice of the speciation model equation/function, with its implicit definition of independent and dependent variables. In “direct modeling”, the dependent variable is the measured [Mf] (or Ip) and the total metal concentration ([M]T) considered independent. In other, much more widely used methods of analyzing titration data – classical linearization, best known as van den Berg/Ružić, and isotherm fitting by nonlinear regression, best known as the Langmuir or Gerringa methods – [Mf] is defined as independent and the dependent variable derived from a calculation that involves both [M]T and [Mf]. Close inspection of the biases and variability in the estimates of ligand parameters and in predictions of ambient [Mf] revealed that the best results were obtained by the first approach. Linear regression of transformed data yielded the largest bias and greatest variability, while non-linear isotherm fitting generated results with mean bias comparable to direct modeling, but also with greater variability. Participants that performed a unified analysis of ACSV titration curves at multiple detection windows for a sample improved their results regardless of the basic mathematical approach taken. Overall, the three most accurate sets of results were obtained using automated-unified analysis while the single most accurate set of results combined simultaneous calibration and parameter estimation. We therefore recommend that where sample volume and time permit, titration experiments for all natural water samples be designed to include two or more detection windows, especially for coastal and estuarine waters. It is vital that even more practical experimental designs for multi-window titrations be developed. In addition, while nearly every mathematical approach can prove to be adequate for some datasets, matrix-based equilibrium models are most naturally suited to the task for all datasets and can most easily handle the challenges encountered in this work, i.e., the cases where the added ligand in ACSV became titrated. The ProMCC program (Omanović et al., this issue) as well as the Excel Add-in based KINETEQL Multiwindow Solver spreadsheet (Hudson, 2014) have this capability and have been made available for public use as a result of this intercalibration exercise.

Transitions in community genomic features and biogeochemical processes were examined in surface and subsurface chlorophyll maximum (SCM) microbial communities across a trophic gradient from mesotrophic waters near San Diego, California to the oligotrophic Pacific. Transect end points contrasted in thermocline depth, rates of nitrogen and CO2 uptake, new production and SCM light intensity. Relative to surface waters, bacterial SCM communities displayed greater genetic diversity and enrichment in putative sulfur oxidizers, multiple actinomycetes, low-light-adapted Prochlorococcus and cell-associated viruses. Metagenomic coverage was not correlated with transcriptional activity for several key taxa within Bacteria. Low-light-adapted Prochlorococcus, Synechococcus, and low abundance gamma-proteobacteria enriched in the>3.0-μm size fraction contributed disproportionally to global transcription. The abundance of these groups also correlated with community functions, such as primary production or nitrate uptake. In contrast, many of the most abundant bacterioplankton, including SAR11, SAR86, SAR112 and high-light-adapted Prochlorococcus, exhibited low levels of transcriptional activity and were uncorrelated with rate processes. Eukaryotes such as Haptophytes and non-photosynthetic Aveolates were prevalent in surface samples while Mamielles and Pelagophytes dominated the SCM. Metatranscriptomes generated with ribosomal RNA-depleted mRNA (total mRNA) coupled to in vitro polyadenylation compared with polyA-enriched mRNA revealed a trade-off in detection eukaryotic organelle and eukaryotic nuclear origin transcripts, respectively. Gene expression profiles of SCM eukaryote populations, highly similar in sequence identity to the model pelagophyte Pelagomonas sp. CCMP1756, suggest that pelagophytes are responsible for a majority of nitrate assimilation within the SCM.

Enhanced vertical carbon transport (gravitational sinking and subduction) at mesoscale ocean fronts may explain the demonstrated imbalance of new production and sinking particle export in coastal upwelling ecosystems. Based on flux assessments from 238U:234Th disequilibrium and sediment traps, we found 2 to 3 times higher rates of gravitational particle export near a deep-water front (305 mg C⋅m-2⋅d-1) compared with adjacent water or to mean (nonfrontal) regional conditions. Elevated particle flux at the front was mechanistically linked to Fe-stressed diatoms and high mesozooplankton fecal pellet production. Using a data assimilative regional ocean model fit to measured conditions, we estimate that an additional ∼225 mg C⋅m-2⋅d-1 was exported as subduction of particle-rich water at the front, highlighting a transport mechanism that is not captured by sediment traps and is poorly quantified by most models and in situ measurements. Mesoscale fronts may be responsible for over a quarter of total organic carbon sequestration in the California Current and other coastal upwelling ecosystems.

Organic dissolved iron (dFe)–binding ligands were measured by competitive ligand exchange–adsorptive cathodic stripping voltammetry (CLE-ACSV) at multiple analytical windows (side reaction coefficient of salicylaldoxime, aFe(SA)2 ~30, 60, and 100) in surface and benthic boundary layer (BBL) samples along the central California coast during spring and summer. The weakest ligands were detected in the BBL at the lowest analytical window with average log K cond FeL,Fe’ ~10:2 + 0:4 in the summer and 10.8 6 0.2 in the spring. Between 3% and 18% of the dFe complexation in the BBL was accounted for by HS, which were measured separately in samples by ACSV and may indicate a source of dFe-binding ligands from San Francisco Bay. The strongest ligands were found in nearshore spring surface waters at the highest analytical window with average log K cond FeL,Fe’~11:9 + 0:3, and the concentrations of these ligands declined rapidly offshore. The ligand pools in the surface and BBL waters were distinct from each other based on principal components analysis, with variances in the BBL ligand pool explained by sample location, and variance in surface waters explained by water mass. The use of multiple analytical window analysis elucidated several distinct iron-binding ligand pools, each with unique distributions in the central California Current system.

Hemes are iron containing heterocyclic molecules important in many cellular processes. In the marine environment, hemes participate as enzymatic cofactors in biogeochemically significant processes like photosynthesis, respiration, and nitrate assimilation. Further, hemoproteins, hemes, and their analogs appear to be iron sources for some marine bacterioplankton under certain conditions. Current oceanographic analytical methodologies allow for the extraction and measurement of heme b from marine material, and a handful of studies have begun to examine the distribution of heme b in ocean basins. The study of heme in the marine environment is still in its infancy, but some trends can be gleaned from the work that has been published so far. In this review, we summarize what is known or might be inferred about the roles of heme in marine microbes as well as the few studies on heme in the marine environment that have been conducted to date. We conclude by presenting some future questions and challenges for the field.

Organic ligands form strong complexes with many trace elements in seawater. Various metals can compete for the same ligand chelation sites, and the final speciation of bound metals is determined by relative binding affinities, concentrations of binding sites, uncomplexed metal concentrations, and association/dissociation kinetics. Different ligands have a wide range of metal affinities and specificities. However, the chemical composition of these ligands in the marine environment remains poorly constrained, which has hindered progress in modeling marine metal speciation. In this study, we detected and characterized natural ligands that bind copper (Cu) and nickel (Ni) in the eastern South Pacific Ocean with liquid chromatography tandem inductively coupled plasma mass spectrometry (LC-ICPMS), and high resolution electrospray ionization mass spectrometry (ESIMS). Dissolved Cu, Ni, and ligand concentrations were highest near the coast. Chromatographically unresolved polar compounds dominated ligands isolated near the coast by solid phase extraction. Offshore, metal and ligand concentrations decreased, but several new ligands appeared. One major ligand was detected that bound both Cu2+ and Ni2+. Based on accurate mass and fragmentation measurements, this compound has a molecular formula of [C20H21N4O8S2 + M]+ (M = metal isotope) and contains several azole-like metal binding groups. Additional lipophilic Ni complexes were also present only in oligotrophic waters, with masses of 649, 698, and 712 m/z (corresponding to the 58Ni metal complex). Molecular formulae of [C32H54N3O6S2Ni]+ and [C33H56N3O6S2Ni]+ were determined for two of these compounds. Addition of Cu and Ni to the samples also revealed the presence of additional compounds that can bind both Ni and Cu. Although these specific compounds represent a small fraction of the total dissolved Cu and Ni pool, they highlight the compositional diversity and spatial heterogeneity of marine Ni and Cu ligands, as well as variability in the extent to which different metals in the same environment compete for ligand binding.

The Antarctic Peninsula (AP) shelf is an important source of dissolved iron (Fe) to the upper ocean in the southern Scotia Sea, one of the most productive regions of the Southern Ocean. Here we present results from a four-year (2003-2006) numerical simulation using a regional coupled physical-biogeochemical model to assess the Fe sources and transport on the AP shelf and toward the southern Scotia Sea. The model was validated with a suite of data derived from in situ surveys and remote sensing. Model results indicate that sediments in the AP shelf and the South Orkney Plateau (SOP) provide the dominant source of Fe to the upper 500 m in the southern Scotia Sea. Additional Fe inputs to the region are associated with the Antarctic Circumpolar Current (ACC) and the northern limb of the Weddell Gyre, deep-ocean sediment sources, dust deposition, and icebergs. Fe on the AP shelf originates primarily from sediments on the relatively shallow inner shelf and is directly injected into the water column and subsequently transported toward Elephant Island by the confluent shelf currents. Off-shelf Fe export is primarily through entrainment of shelf waters by the ACC’s Southern Boundary frontal jet along the northern edge of the AP shelf, the Hesperides Trough, and the SOP shelf. About 70% of the off-shelf export takes place below the surface mixed layer, and is subsequently re-supplied to the euphotic zone through vertical mixing, mainly during austral fall and winter. The exported shelf-derived Fe is then advected downstream by the ACC and Weddell Gyre and spread over the southern and eastern Scotia Seas. Taken together, shelf Fe export witin top 500 m meets nearly all of the Fe demand of phytoplankton photosynthesis in the southern Scotia Sea. Waters with elevated Fe concentrations in the Scotia Sea are largely restricted to south of the Southern ACC Front.

The bioavailability and utilization of porphyrin-bound iron, specifically heme, by marine microorganisms have rarely been examined. This study used Ruegeria sp. strain TrichCH4B as a model organism to study heme acquisition by a member of the Roseobacter clade. Analogs of known heme transporter proteins were found within the Ruegeria sp. TrichCH4B genome. The identified heme uptake and utilization system appears to be functional, as the heme genes were upregulated under iron stress, the bacterium could grow on ferric-porphyrin complexes as the sole iron source, and internalization of 55 Fe from ferric protoporphyrin IX was observed. The potential ability to utilize heme in the Roseobacter clade appears to be common, as half of the isolates in the RoseoBase database were found to have a complete heme uptake system. A degenerate primer set was designed and successfully used to identify the putative heme oxygenase gene ( hmus ) in the roseobacter heme uptake system from diverse nonenriched marine environments. This study found that members of the Roseobacter clade are capable of utilizing heme as an iron source and that this capability may be present in all types of marine environments. The results of this study add a new perspective to the current picture of iron cycling in marine systems, whereby relatively refractory intracellular pools of heme-bound iron may be taken up quickly and directly reincorporated into living bacteria without previous degradation or the necessity of a siderophore intermediate.

The southern California Current Ecosystem (CCE) is a dynamic eastern boundary current ecosystem that is forced by ocean-atmosphere variability on interannual, multidecadal, and long-term secular time scales. Recent evidence suggests that apparent abrupt transitions in ecosystem conditions reflect linear tracking of the physical environment rather than oscillations between alternative preferred states. A space-for-time exchange is one approach that permits use of natural spatial variability in the CCE to develop a mechanistic understanding needed to project future temporal changes. The role of (sub)mesoscale frontal systems in altering rates of nutrient transport, primary and secondary production, export fluxes, and the rates of encounters between predators and prey is an issue central to this pelagic ecosystem and its future trajectory because the occurrence of such frontal features is increasing. © 2013 by The Oceanography Society. All rights reserved.

Copper-based epoxy and ablative antifouling painted panels were exposed in natural seawater to evaluate environmental loading parameters. In situ loading factors including initial exposure, passive leaching, and surface refreshment were measured utilizing two protocols developed by the US Navy: the dome method and the in-water hull cleaning sampling method. Cleaning techniques investigated included a soft-pile carpet and a medium duty 3M(™) pad for fouling removal. Results show that the passive leach rates of copper peaked three days after both initial deployment and cleaning events (CEs), followed by a rapid decrease over about 15 days and a slow approach to asymptotic levels on approximately day 30. Additionally, copper was more bioavailable during a CE in comparison to the passive leaching that immediately followed. A paint life cycle model quantifying annual copper loading estimates for each paint and cleaning method based on a three-year cycle of painting, episodic cleaning, and passive leaching is presented.

Copper-binding organic ligands were measured during austral winter in surface waters around the Antarctic Peninsula using competitive ligand exchange-adsorptive cathodic stripping voltammetry with multiple analytical windows. Samples were collected from four distinct water masses including the Antarctic Circumpolar Current, Southern Antarctic Circumpolar Current Front, Bransfield Strait, and the shelf region of the Antarctic Peninsula. Strong copper-binding organic ligands were detected in each water mass. The strongest copper-binding ligands were detected at the highest competition strength in the Antarctic Circumpolar Current, with an average conditional stability constant of log K CuL , Cu 2 + c o n d = 16.00 ± 0 . 82 . The weakest ligands were found at the lowest competition strength in the shelf region with log K CuL , Cu 2 + c o n d = 12 . 68 ± 0 . 48 . No ligands with stability constants less than log K CuL , Cu 2 + c o n d = 13.5 were detected in the Antarctic Circumpolar Current at any competition strength, suggesting a shelf source of weaker copper-binding ligands. Free, hydrated copper ion concentrations, the biologically available form of dissolved copper, were less than 10−14 M in all samples, approaching levels that may be limiting for some types of inducible iron acquisition.

Iron (Fe) is the limiting nutrient for primary productivity in the Southern Ocean, with much of the dissolved iron (dFe) bound to organic ligands or colloids. A Fe model for the Southern Ocean (SOFe) is developed to understand the role of bacteria and organic ligands in controlling Fe cycling and productivity. The model resolves the classical food web and microbial loop, including three types of nutrients (N, Si, Fe) and two types of Fe ligands. Simulations of the zero-dimensional (0-D) model are calibrated with detailed results of shipboard grow-out incubation experiments conducted with Antarctic Peninsula phytoplankton communities during winter 2006 to provide the best estimate of key biological parameters. Then a one-dimensional (1-D) model is developed by coupling the biological model with the Regional Oceanic Modeling System (ROMS) for a site on the Antarctic Peninsula shelf, and the model parameters are further calibrated with data collected from two surveys (summer 2004 and winter 2006) in the area. The results of the numerical simulations agree reasonably well with observations. An analysis of the 1-D model results suggests that bacteria and organic ligands may play an important role in Fe cycling, which can be categorized into a relatively fast mode within the euphotic zone dominated by photo-reactions (summer d Fe residence time about 600 days) and complexation and a slow mode below with most of the dFe biologically complexed (summer dFe residence time >10 years). The dFe removal from the euphotic zone is dominated by colloidal formation and further aggregations with additional contribution from biological uptake, and an increase of organic ligands would reduce Fe export. The decrease of Fe removal rate over depth is due to the continuous dissolution and remineralization of particulate Fe. A number of sensitivity experiments are carried out for both 0-D and 1-D models to understand the importance of photo-reactive processes in primary productivity, bacterial activity, Fe speciation, and dFe residence time within the euphotic zone. The bio-availability of ligand-bound Fe (FeL) is critical to modeled high primary productivity, which is consistent with both shipboard measurements and field observations. In addition, model productivity is sensitive to photoreaction rates if FeL is not directly available for phytoplankton uptake.

The carbon to iron (C:Fe) ratio of planktonic biomass constrains net production in iron-limited regions of the ocean and is an important parameter for predicting biomass production from iron inputs. On a cruise to the southern Drake Passage in July–August 2006, we used two approaches to determine the C:Fe ratio of planktonic material: dual-radiotracer labeling and net biomass production in iron-limited grow-out experiments. There was variability in C:Fe ratios among experiments, but values from the two methods overlapped with average values of 1.4×10 5 (mol:mol) for the radiotracer method and 1.7×10 5 for the net biomass production method. This is notable since the net biomass production method is a new approach to determine C:Fe ratios. Although it has potential issues related to bottle effects and sensitivity to trace contamination, the method avoids some of the questions associated with iron speciation and bioavailability since ambient iron supports production. Because light intensity is known to affect C:Fe ratios in phytoplankton through photosynthetic iron demands, we tested the effect of light level on C:Fe in Antarctic assemblages. In contrast to what is seen in many phytoplankton cultures, C:Fe ratios increased at low-light, but we suspect that this is due to initial photoinhibition of the low-light adapted winter assemblages at higher light levels.

Microbial copper (Cu) nutrition and dissolved Cu speciation were surveyed along Line P, a coastal to open ocean transect that extends from the coast of British Columbia, Canada, to the high-nutrient-low-chlorophyll (HNLC) zone of the northeast subarctic Pacific Ocean. Steady-state size fractionated Cu uptake rates and Cu:C assimilation ratios were determined at in situ Cu concentrations and speciation using a 67Cu tracer method. The cellular Cu:C ratios that we measured (~30 µmol Cu mol C-1) are similar to recent estimates using synchrotron x-ray fluorescence (SXRF), suggesting that the 67Cu method can determine in situ metabolic Cu demands. We examined how environmental changes along the Line P transect influenced Cu metabolism in the sub-microplankton community. Cellular Cu:C assimilation ratios and uptake rates were compared with net primary productivity, bacterial abundance and productivity, total dissolved Cu, Cu speciation, and a suite of other chemical and biological parameters. Total dissolved Cu concentrations ([Cu]d) were within a narrow range (1.46 to 2.79 nM), and Cu was bound to a ~5-fold excess of strong ligands with conditional stability constants ( ) of ~1014. Free Cu2+ concentrations were low (pCu 14.4 to 15.1), and total and size fractionated net primary productivity (NPPV; µg C L-1 d-1) were negatively correlated with inorganic Cu concentrations ([Cu′]). We suggest this is due to greater Cu′ drawdown by faster growing phytoplankton populations. Using the relationship between [Cu′] drawdown and NPPV, we calculated a regional photosynthetic Cu:C drawdown export ratio between 1.5 and 15 µmol Cu mol C-1, and a mixed layer residence time (2.5 to 8 years) that is similar to other independent estimates (2-12 years). Total particulate Cu uptake rates were between 22 and 125 times faster than estimates of Cu export; this is possibly mediated by rapid cellular Cu uptake and efflux by phytoplankton and bacteria or the effects of grazers and bacterial remineralization on dissolved Cu. These results provide a more detailed understanding of the interactions between Cu speciation and microorganisms in seawater, and present evidence that marine phytoplankton modify Cu speciation in the open ocean.

Characterization of the speciation of iron and copper is an important objective of the GEOTRACES Science Plan. To incorporate speciation measurements into such a multinational program, standard practices must be adopted that allow data from multiple labs to be synthesized. Competitive ligand exchange-adsorptive cathodic stripping voltammetry (CLE-ACSV) is the primary technique employed for measuring metal-binding ligands and determining metal speciation in seawater. The determination of concentrations and conditional stability constants of metal-binding ligands is particularly challenging, as results can be influenced both by experimental conditions and interpretation of titration data. Here, we report an investigation between four laboratories to study the speciation of iron and copper using CLE-ACSV. Samples were collected on the GEOTRACES II intercomparison cruise in the North Pacific Ocean in May 2009 at 30° N, 140° W. This intercomparison was carried out shipboard and included an assessment of the viability of sample preservation by freezing. Results showed that consensus values could be obtained between different labs, but that some existing practices were problematic and require further attention in future work. A series of recommendations emerged from this study that will be useful in implementing multi-investigator programs like GEOTRACES.

The distribution and speciation of dissolved Fe (dFe) were measured during four quasi-Lagrangian drogued drifter studies (~ 4 d duration each) that were conducted in the southern California Current System in May 2006 and April 2007. Three of the four drifter studies were within the coastal upwelling regime and one drifter study was in a warm-core anticyclonic eddy. Incubation bottle experiments were also conducted to determine the degree of phytoplankton Fe limitation and to assess changes in the concentration of Fe-binding ligands. In the coastal upwelling drifter studies, in situ dFe (1.4–1.8 nM) and macronutrients were initially high and declined over time. Fe addition incubation experiments indicated that the phytoplankton community was not Fe limited at the beginning of the coastal upwelling drifter experiments (when μM nitrate:nM dFe ratios were ~ 7–8). By the end of two of the three drifter studies (when μM nitrate:nM dFe ratios were ~ 12–19), Fe addition resulted in larger nitrate and silicic acid drawdown, and larger accumulations in chlorophyll a, particulate organic carbon and nitrogen, and diatom and dinoflagellate-specific carotenoid pigments. Fe speciation was measured in situ in three of the four drifter studies with stronger L 1 -type ligands found to be present in excess of dFe in all samples. In Fe speciation incubation experiments, L 1 -type ligand production was observed in conjunction with phytoplankton growth under Fe-limiting conditions. The results presented here support and add a quasi-Lagrangian perspective to previous observations of dFe and macronutrient cycling over space and time within the California coastal upwelling regime, including Fe limitation within the phytoplankton community in this region and the biological production of Fe-binding ligands concomitant with Fe limitation.

Trichodesmium colonies contain an abundant microbial consortium that is likely to play a role in nutrient cycling within the colony. This study used laboratory cultures of Trichodesmium and two genome‐sequenced strains of bacteria typical of Trichodesmium‐associated microbes to develop an understanding of the cycling of iron, a potentially limiting micronutrient, within Trichodesmium colonies. We found that the ferric siderophores desferrioxamine B and aerobactin were not readily bioavailable to Trichodesmium, relative to ferric chloride or citrate‐associated iron. In contrast, the representative bacterial strains we studied were able to acquire iron from all of the iron sources, implying that naturally occurring Trichodesmium‐associated bacteria may be capable of utilizing a more diverse array of iron sources than Trichodesmium. From the organism‐specific uptake data collected in this study, a theoretical Trichodesmium colony was designed to model whole colony iron uptake. The bacteria accounted for most (> 70%) of the iron acquired by the colony, highlighting the importance of determining organism‐specific uptake in a complex environment. Our findings suggest that, although they may share the same micro‐environment, Trichodesmium and its colony‐associated microbial cohort may differ substantially in terms of iron acquisition strategy.

Summary In the pelagic environment, iron is a scarce but essential micronutrient. The iron acquisition capabilities of selected marine bacteria have been investigated, but the recent proliferation of marine prokaryotic genomes and metagenomes offers a more comprehensive picture of microbial iron uptake pathways in the ocean. Searching these data sets, we were able to identify uptake mechanisms for Fe3+, Fe2+ and iron chelates (e.g. siderophore and haem iron complexes). Transport of iron chelates is accomplished by TonB-dependent transporters (TBDTs). After clustering the TBDTs from marine prokaryotic genomes, we identified TBDT clusters for the transport of hydroxamate and catecholate siderophore iron complexes and haem using gene neighbourhood analysis and co-clustering of TBDTs of known function. The genomes also contained two classes of siderophore biosynthesis genes: NRPS (non-ribosomal peptide synthase) genes and NIS (NRPS Independent Siderophore) genes. The most common iron transporters, in both the genomes and metagenomes, were Fe3+ ABC transporters. Iron uptake-related TBDTs and siderophore biosynthesis genes were less common in pelagic marine metagenomes relative to the genomic data set, in part because Pelagibacter ubique and Prochlorococcus species, which almost entirely lacked these Fe uptake systems, dominate the metagenomes. Our results are largely consistent with current knowledge of iron speciation in the ocean, but suggest that in certain niches the ability to acquire siderophores and/or haem iron chelates is beneficial.

The evolution of dissolved iron (Fe) and copper (Cu) speciation was followed through a simulated spring bloom event in a 15-day incubation experiment of natural seawater collected during austral winter from high macronutrient high Fe waters of Bransfield Strait in the Southern Ocean. The incubation experiment included unamended bottles as well as Fe additions using the stable isotope of Fe, 57Fe, as inorganic (57FeCl3) and organic (57Fe-aerobactin, 57Fe-desferrioxamine B) amendments. Exposure to summer light conditions resulted in substantial growth for all treatments, mimicking the initiation of a spring bloom. The addition of Fe resulted in a 30% increase in phytoplankton biomass over unamended controls by day 15, indicating that the unamended waters became Fe limited despite initially elevated dissolved Fe concentrations. Dissolved Cu and Cu speciation remained largely unchanged for all treatments of the incubation, with Cu speciation dominated by exceedingly strong Cu-binding ligands (log KCuL1,Cu2+cond ~ 16) and low resultant Cu2+ concentrations (10− 16.3 ± 0.3 mol L− 1). In only the unamended light bottles, strong Fe-binding ligands were produced over the course of the experiment. The observed production of strong Fe-binding ligands in the control bottles that became Fe-limited supports the important role of biologically produced siderophore-type natural ligands in the marine Fe cycle.

In most oceanic environments, dissolved nickel (Ni) concentrations are drawn down in surface waters with increasing concentrations at depth, implying a role for biology in the geochemical distribution of Ni. Studies with phytoplankton isolates from the surface ocean have established the biochemical roles of Ni in the assimilation of urea and oxidative defense. To determine if these requirements are relevant in natural marine planktonic assemblages, bottle-based fertilization experiments were used to test the effects of low-level additions of Ni, urea, or both Ni and urea to surface waters at several locations offshore of Peru and California, as well as in the Gulf of California. Urea and Ni+urea additions consistently promoted phytoplankton growth relative to control and +Ni treatments, except in a coastal upwelling site and Peruvian water. No effect was observed in the upwelling site, but in Peruvian waters urea additions resulted in increased phytoplankton pigments and phosphate drawdown only when Ni was added concurrently, suggesting a biochemically dependent Ni–urea colimitation. In the Gulf of California, Ni additions without urea resulted in increased abundances of cyanobacteria, picoeukaryotes, and the corresponding pigments. As urea additions showed the overall phytoplankton community was also urea-limited, it appears that the cyanobacteria and potentially the picoeukaryotes were colimited by Ni and urea in a biochemically independent fashion. In parallel, radiotracer-based uptake experiments were used to study the kinetics and spatial variation of biological Ni assimilation. In these experiments, the added radiotracer rarely equilibrated with the natural Ni present, precluding estimates a determination of in situ Ni uptake rates and suggesting that much of the natural Ni was not bioavailable. The lack of equilibration likely did not preclude the measurement of community Ni uptake kinetics, nor the comparison of measured rates between locations. The highest VmaxKρ−1 values, which reflect a competitive advantage in Ni acquisition at low concentrations, were observed in stratified nitrogen-deplete communities, potentially linking Ni and nitrogen biogeochemistry in a manner consistent with the biochemical utilization of Ni. Overall, uptake rates were higher in the euphotic rather than non-euphotic zone communities, directly reconciling the nutrient-like depth profile of Ni. The Ni uptake rates observed at the nitrate-replete Fe-deplete Peru stations were an order of magnitude lower than the other sites. This result agrees with calculations suggesting that saturation of the cell surface with Ni and iron (Fe) transporters may limit uptake rates in low Fe waters.

The ability to acquire diverse and abundant forms of iron would be expected to confer a survival advantage in the marine environment, where iron is scarce. Marine bacteria are known to use siderophores and inorganic iron, but their ability to use heme, an abundant intracellular iron form, has only been examined preliminarily. Microscilla marina , a cultured relative of a bacterial group frequently found on marine particulates, was used as a model organism to examine heme uptake. Searches of the genome revealed analogs to known heme transport proteins, and reverse transcription-quantitative PCR analysis of these genes showed that they were expressed and upregulated under iron stress and during growth on heme. M. marina was found to take up heme-bound iron and could grow on heme as a sole iron source, supporting the genetic evidence for heme transport. Similar putative heme transport components were identified in the genomes of diverse marine bacteria. These systems were found in the genomes of many bacteria thought to be particle associated but were lacking in known free-living organisms (e.g., Pelagibacter ubique and marine cyanobacteria). This distribution of transporters is consistent with the hydrophobic, light-sensitive nature of heme, suggesting that it is primarily available on phytoplankton or detritus or in nutrient-rich environments.

The roles of iron and light as limiting and colimiting factors for phytoplankton growth in subsurface chlorophyll maxima (SCMs) were investigated in mesotrophic to oligotrophic waters of the Southern California Bight and the eastern tropical North Pacific using microcosm manipulation experiments. Phytoplankton responses indicative of iron–light colimitation were found at several SCMs underlying macronutrient-limited surface waters in the eastern Pacific. Iron additions led to a shift in the size and taxonomic structure of the phytoplankton community, where large diatoms dominated what was formerly a diverse community of relatively small phytoplankton. The strongest and most ubiquitous responses of diatoms to iron addition were found under elevated light conditions, indicating that iron availability may have the greatest potential to affect SCM phytoplankton communities when light levels increase rapidly, such as during eddy events or with strong internal waves. The results show that iron influences phytoplankton community structure at SCMs, which would have consequences for nutrient cycling and carbon export within the lower euphotic zone. It is now well established that iron can control phytoplankton biomass and productivity in high nutrient–low chlorophyll (HNLC) regions, where unused macronutrients are persistently present in surface waters. More recently, the importance of iron availability for phytoplankton has been shown in waters outside of HNLC areas. In coastal upwelling zones, rapid movement of high