The cobalt cycle in the Tropical Pacific Ocean

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February 2017Although over a dozen elements are needed to support phytoplankton growth, only a few are considered to be growth-limiting. As the central atom in vitamin B12, cobalt is crucial for metabolism, but its status as a limiting nutrient is uncertain. This thesis investigates the geochemical controls on oceanic cobalt scarcity and their biological consequences. Analysis of over 1000 samples collected in the Tropical Pacific Ocean reveals a dissolved cobalt distribution that is strongly coupled to dissolved oxygen, with peak concentrations where oxygen is lowest. Large cobalt plumes within anoxic waters are maintained by three processes: 1) a cobalt supply from organic matter remineralization, 2) an amplified sedimentary source from oxygen-depleted coastlines, and 3) low-oxygen inhibition of manganese oxidation, which scavenges cobalt from the water column. Rates of scavenging are calculated from a global synthesis of recent GEOTRACES data and agree with cobalt accumulation rates in pelagic sediments. Because both sources and sinks are tied to the extent of oxygen minimum zones, oceanic cobalt inventories are likely dynamic on the span of decades. Despite extremely low cobalt in the South Pacific gyre, the cyanobacterium Prochlorococcus thrives. Minimum cobalt and iron requirements of a Prochlorococcus strain isolated from the Equatorial Pacific are quantified. Cobalt quotas are related to demand for ribonucleotide reductase and methionine synthase enzymes, which catalyze critical steps in DNA and protein biosynthesis, respectively. Compared to other cyanobacteria, a streamlined metal physiology makes Prochlorococcus susceptible to competitive inhibition of cobalt uptake by low levels of zinc. Although phytoplankton in the Equatorial Pacific are subject to chronic iron-limitation, widespread cobalt scarcity and vulnerability to zinc inhibition observed in culture imply that wild Prochlorococcus are not far from a cobalt-limitation threshold.I am lucky to have benefitted from major financial support of the Saito Lab by the National Science Foundation and the Gordon and Betty Moore Foundation. Specifically, National Science Foundation grants for the Center for Microbial Oceanography Research and Education (CMORE, DBI-0424599), GEOTRACES Pacific and Artic projects (OCE-1233261 and OCE- 1540254), and OCE-1220484 funded my thesis work. National Science Foundation grants OCE- 1031271 and OCE-1337780 and Gordon and Betty Moore Foundation grants 3782 and 3934 to the Saito lab also provided instrumentation and funded field expeditions that enabled this work

Structural characterization of natural nickel and copper binding ligands along the US GEOTRACES Eastern Pacific Zonal Transect

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Frontiers in Marine Science 3 (2016): 243, doi:10.3389/fmars.2016.00243.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.Support was provided by the National Science Foundation (NSF) program in Chemical Oceanography (OCE-1356747, OCE-1233261, OCE-1233733, OCE-1233502, and OCE-1237034), the NSF Science and Technology Center for Microbial Oceanography Research and Education (C-MORE; DBI-0424599), the Gordon and Betty Moore Foundation (#3298 and 3934), and the Simons Foundation (#329108, DR)

Coastal sources, sinks and strong organic complexation of dissolved cobalt within the US North Atlantic GEOTRACES transect GA03

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 14 (2017): 2715-2739, doi:10.5194/bg-14-2715-2017.Cobalt is the scarcest of metallic micronutrients and displays a complex biogeochemical cycle. This study examines the distribution, chemical speciation, and biogeochemistry of dissolved cobalt during the US North Atlantic GEOTRACES transect expeditions (GA03/3_e), which took place in the fall of 2010 and 2011. Two major subsurface sources of cobalt to the North Atlantic were identified. The more prominent of the two was a large plume of cobalt emanating from the African coast off the eastern tropical North Atlantic coincident with the oxygen minimum zone (OMZ) likely due to reductive dissolution, biouptake and remineralization, and aeolian dust deposition. The occurrence of this plume in an OMZ with oxygen above suboxic levels implies a high threshold for persistence of dissolved cobalt plumes. The other major subsurface source came from Upper Labrador Seawater, which may carry high cobalt concentrations due to the interaction of this water mass with resuspended sediment at the western margin or from transport further upstream. Minor sources of cobalt came from dust, coastal surface waters and hydrothermal systems along the Mid-Atlantic Ridge. The full depth section of cobalt chemical speciation revealed near-complete complexation in surface waters, even within regions of high dust deposition. However, labile cobalt observed below the euphotic zone demonstrated that strong cobalt-binding ligands were not present in excess of the total cobalt concentration there, implying that mesopelagic labile cobalt was sourced from the remineralization of sinking organic matter. In the upper water column, correlations were observed between total cobalt and phosphate, and between labile cobalt and phosphate, demonstrating a strong biological influence on cobalt cycling. Along the western margin off the North American coast, this correlation with phosphate was no longer observed and instead a relationship between cobalt and salinity was observed, reflecting the importance of coastal input processes on cobalt distributions. In deep waters, both total and labile cobalt concentrations were lower than in intermediate depth waters, demonstrating that scavenging may remove labile cobalt from the water column. Total and labile cobalt distributions were also compared to a previously published South Atlantic GEOTRACES-compliant zonal transect (CoFeMUG, GAc01) to discern regional biogeochemical differences. Together, these Atlantic sectional studies highlight the dynamic ecological stoichiometry of total and labile cobalt. As increasing anthropogenic use and subsequent release of cobalt poses the potential to overpower natural cobalt signals in the oceans, it is more important than ever to establish a baseline understanding of cobalt distributions in the ocean.We also gratefully acknowledge support of funding agencies on the following grants: the US National Science Foundation (NSF-OCE 0928414, 1233261, 1435056) and the Gordon and Betty Moore Foundation (grant 3738)

A dissolved cobalt plume in the oxygen minimum zone of the eastern tropical South Pacific

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 13 (2016): 5697-5717, doi:10.5194/bg-13-5697-2016.Cobalt is a nutrient to phytoplankton, but knowledge about its biogeochemical cycling is limited, especially in the Pacific Ocean. Here, we report sections of dissolved cobalt and labile dissolved cobalt from the US GEOTRACES GP16 transect in the South Pacific. The cobalt distribution is closely tied to the extent and intensity of the oxygen minimum zone in the eastern South Pacific with highest concentrations measured at the oxycline near the Peru margin. Below 200 m, remineralization and circulation produce an inverse relationship between cobalt and dissolved oxygen that extends throughout the basin. Within the oxygen minimum zone, elevated concentrations of labile cobalt are generated by input from coastal sources and reduced scavenging at low O2. As these high cobalt waters are upwelled and advected offshore, phytoplankton export returns cobalt to low-oxygen water masses underneath. West of the Peru upwelling region, dissolved cobalt is less than 10 pM in the euphotic zone and strongly bound by organic ligands. Because the cobalt nutricline within the South Pacific gyre is deeper than in oligotrophic regions in the North and South Atlantic, cobalt involved in sustaining phytoplankton productivity in the gyre is heavily recycled and ultimately arrives from lateral transport of upwelled waters from the eastern margin. In contrast to large coastal inputs, atmospheric deposition and hydrothermal vents along the East Pacific Rise appear to be minor sources of cobalt. Overall, these results demonstrate that oxygen biogeochemistry exerts a strong influence on cobalt cycling.This work was funded by NSF awards OCE-1233733 to MAS, OCE-1232814 to BST, and OCE-1237011 to JAR

Siderophore-Based Microbial Adaptations to Iron Scarcity Across the Eastern Pacific Ocean

Nearly all iron dissolved in the ocean is complexed by strong organic ligands of unknown composition. The effect of ligand composition on microbial iron acquisition is poorly understood, but amendment experiments using model ligands show they can facilitate or impede iron uptake depending on their identity. Here we show that siderophores, organic compounds synthesized by microbes to facilitate iron uptake, are a dynamic component of the marine ligand pool in the eastern tropical Pacific Ocean. Siderophore concentrations in iron-deficient waters averaged 9 pM, up to fivefold higher than in iron-rich coastal and nutrient-depleted oligotrophic waters, and were dominated by amphibactins, amphiphilic siderophores with cell membrane affinity. Phylogenetic analysis of amphibactin biosynthetic genes suggests that the ability to produce amphibactins has transferred horizontally across multiple Gammaproteobacteria, potentially driven by pressures to compete for iron. In coastal and oligotrophic regions of the eastern Pacific Ocean, amphibactins were replaced with lower concentrations (1-2 pM) of hydrophilic ferrioxamine siderophores. Our results suggest that organic ligand composition changes across the surface ocean in response to environmental pressures. Hydrophilic siderophores are predominantly found across regions of the ocean where iron is not expected to be the limiting nutrient for the microbial community at large. However, in regions with intense competition for iron, some microbes optimize iron acquisition by producing siderophores that minimize diffusive losses to the environment. These siderophores affect iron bioavailability and thus may be an important component of the marine iron cycle

Recycling of dissolved iron in the North Pacific Subtropical Gyre

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hawco, N. J., Yang, S.-C., Pinedo-Gonzalez, P., Black, E. E., Kenyon, J., Ferron, S., Bian, X., & John, S. G. Recycling of dissolved iron in the North Pacific Subtropical Gyre. Limnology and Oceanography, 67(11), (2022): 2448-2465, https://doi.org/10.1002/lno.12212.The importance of iron as a limiting nutrient in the open ocean is widely recognized, but there is substantial uncertainty about the rate that it cycles in the marine environment. Here, we combine measurements from the water column, sediment traps, and incubations to constrain Fe turnover during summer at Station ALOHA in the North Pacific Subtropical Gyre. Using low levels of 57Fe–58Fe double spike, measured with high precision by multi-collector inductively coupled plasma mass spectrometry, we find Fe uptake rates of 30–60 pM d−1 throughout the euphotic zone. Dissolved Fe turnover times are estimated at 10–15 d in the mixed layer and 1–3 d near the deep chlorophyll maximum. Aerosol Fe supply inferred from a thorium isotope mass balance indicates that the dissolved Fe residence time is approximately 6 months in the upper euphotic zone (0–75 m), relative to external sources, and 2 months in the lower euphotic zone (75–150 m). To reconcile these observations, the average Fe atom must be recycled over 25 times at Station ALOHA in both the upper and lower euphotic zones (an “Fe ratio” equal to 0.04 and 0.03, respectively), a level of conservation that has only been documented in Fe-limited regions thus far. At steady state, this scenario requires an aerosol Fe solubility of 4.5%, which is similar to dissolution experiments from Pacific Ocean aerosols. Our results suggest that the oligotrophic ocean is capable of recycling iron efficiently even when these ecosystems are not demonstrably iron-limited.This work was also supported by the Simons Foundation (602538 and 823167 to N.J.H., 329108 to S.G.J) and National Science Foundation grants 2022969 to N.J.H. and 1911990 to S.F

Coastal sources, sinks and strong organic complexation of dissolved cobalt within the US North Atlantic GEOTRACES transect GA03

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 14 (2017): 2715-2739, doi:10.5194/bg-14-2715-2017.Cobalt is the scarcest of metallic micronutrients and displays a complex biogeochemical cycle. This study examines the distribution, chemical speciation, and biogeochemistry of dissolved cobalt during the US North Atlantic GEOTRACES transect expeditions (GA03/3_e), which took place in the fall of 2010 and 2011. Two major subsurface sources of cobalt to the North Atlantic were identified. The more prominent of the two was a large plume of cobalt emanating from the African coast off the eastern tropical North Atlantic coincident with the oxygen minimum zone (OMZ) likely due to reductive dissolution, biouptake and remineralization, and aeolian dust deposition. The occurrence of this plume in an OMZ with oxygen above suboxic levels implies a high threshold for persistence of dissolved cobalt plumes. The other major subsurface source came from Upper Labrador Seawater, which may carry high cobalt concentrations due to the interaction of this water mass with resuspended sediment at the western margin or from transport further upstream. Minor sources of cobalt came from dust, coastal surface waters and hydrothermal systems along the Mid-Atlantic Ridge. The full depth section of cobalt chemical speciation revealed near-complete complexation in surface waters, even within regions of high dust deposition. However, labile cobalt observed below the euphotic zone demonstrated that strong cobalt-binding ligands were not present in excess of the total cobalt concentration there, implying that mesopelagic labile cobalt was sourced from the remineralization of sinking organic matter. In the upper water column, correlations were observed between total cobalt and phosphate, and between labile cobalt and phosphate, demonstrating a strong biological influence on cobalt cycling. Along the western margin off the North American coast, this correlation with phosphate was no longer observed and instead a relationship between cobalt and salinity was observed, reflecting the importance of coastal input processes on cobalt distributions. In deep waters, both total and labile cobalt concentrations were lower than in intermediate depth waters, demonstrating that scavenging may remove labile cobalt from the water column. Total and labile cobalt distributions were also compared to a previously published South Atlantic GEOTRACES-compliant zonal transect (CoFeMUG, GAc01) to discern regional biogeochemical differences. Together, these Atlantic sectional studies highlight the dynamic ecological stoichiometry of total and labile cobalt. As increasing anthropogenic use and subsequent release of cobalt poses the potential to overpower natural cobalt signals in the oceans, it is more important than ever to establish a baseline understanding of cobalt distributions in the ocean.We also gratefully acknowledge support of funding agencies on the following grants: the US National Science Foundation (NSF-OCE 0928414, 1233261, 1435056) and the Gordon and Betty Moore Foundation (grant 3738)

Minimal cobalt metabolism in the marine cyanobacterium Prochlorococcus.

Despite very low concentrations of cobalt in marine waters, cyanobacteria in the genus Prochlorococcus retain the genetic machinery for the synthesis and use of cobalt-bearing cofactors (cobalamins) in their genomes. We explore cobalt metabolism in a Prochlorococcus isolate from the equatorial Pacific Ocean (strain MIT9215) through a series of growth experiments under iron- and cobalt-limiting conditions. Metal uptake rates, quantitative proteomic measurements of cobalamin-dependent enzymes, and theoretical calculations all indicate that Prochlorococcus MIT9215 can sustain growth with less than 50 cobalt atoms per cell, ∼100-fold lower than minimum iron requirements for these cells (∼5,100 atoms per cell). Quantitative descriptions of Prochlorococcus cobalt limitation are used to interpret the cobalt distribution in the equatorial Pacific Ocean, where surface concentrations are among the lowest measured globally but Prochlorococcus biomass is high. A low minimum cobalt quota ensures that other nutrients, notably iron, will be exhausted before cobalt can be fully depleted, helping to explain the persistence of cobalt-dependent metabolism in marine cyanobacteria

Manganese Limitation of Phytoplankton Physiology and Productivity in the Southern Ocean

Although iron and light are understood to regulate the Southern Ocean biological carbon pump, observations have also indicated a possible role for manganese. Low concentrations in Southern Ocean surface waters suggest manganese limitation is possible, but its spatial extent remains poorly constrained and direct manganese limitation of the marine carbon cycle has been neglected by ocean models. Here, using available observations, we develop a new global biogeochemical model and find that phytoplankton in over half of the Southern Ocean cannot attain maximal growth rates because of manganese deficiency. Manganese limitation is most extensive in austral spring and depends on phytoplankton traits related to the size of photosynthetic antennae and the inhibition of manganese uptake by high zinc concentrations in Antarctic waters. Importantly, manganese limitation expands under the increased iron supply of past glacial periods, reducing the response of the biological carbon pump. Overall, these model experiments describe a mosaic of controls on Southern Ocean productivity that emerge from the interplay of light, iron, manganese and zinc, shaping the evolution of Antarctic phytoplankton since the opening of the Drake Passage