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Abstract. Zinc (Zn) is an essential micronutrient for most eukaryotic phytoplankton. Zn uptake by phytoplankton within the euphotic zone results in nutrient-like dissolved Zn (dZn) profiles with a large dynamic range. The combination of key biochemical uses for Zn and large vertical gradients in dZn implies the potential for rapid rates of Zn removal from the surface ocean. However, due to the ease of contamination at sea, direct measurements of dZn uptake within natural environments have not been previously made. To investigate the demand for dZn and for dissolved cadmium (dCd; a closely related nutrient-like element) within Southern Ocean phytoplankton communities, we conducted 67Zn and 110Cd tracer uptake experiments within the Amundsen Sea, Ross Sea, and Terra Nova Bay of the Southern Ocean. We observed a high magnitude of Zn uptake (ρZn > 100 pmol dZn L−1 d−1) into the particulate phase that was consistent with ambient depleted dZn surface concentrations. High biomass and low partial pressure of carbon dioxide in seawater (seawater pCO2) appeared to contribute to ρZn, which also led to increases in ρCd likely through the upregulation of shared transport systems. These high ρZn measurements further imply that only short timescales are needed to deplete the large winter dZn inventory down to the observed surface levels in this important carbon-capturing region. Overall, the high magnitude of Zn uptake into the particulate fraction suggests that even in the Zn-rich waters of the Southern Ocean, high Zn uptake rates can lead to Zn depletion and potential Zn scarcity. 

Abstract Scarce dissolved surface ocean concentrations of the essential algal micronutrient zinc suggest that Zn may influence the growth of phytoplankton such as diatoms, which are major contributors to marine primary productivity. However, the specific mechanisms by which diatoms acclimate to Zn deficiency are poorly understood. Using global proteomic analysis, we identified two proteins (ZCRP-A/B, Zn/Co Responsive Protein A/B) among four diatom species that became abundant under Zn/Co limitation. Characterization using reverse genetic techniques and homology data suggests putative Zn/Co chaperone and membrane-bound transport complex component roles for ZCRP-A (a COG0523 domain protein) and ZCRP-B, respectively. Metaproteomic detection of ZCRPs along a Pacific Ocean transect revealed increased abundances at the surface (<200 m) where dZn and dCo were scarcest, implying Zn nutritional stress in marine algae is more prevalent than previously recognized. These results demonstrate multiple adaptive responses to Zn scarcity in marine diatoms that are deployed in low Zn regions of the Pacific Ocean. 

Abstract Antarctic Bottom Water (AABW) supplies the lower limb of the global overturning circulation and ventilates the abyssal ocean. In recent decades, AABW has warmed, freshened and reduced in volume. Ross Sea Bottom Water (RSBW), the second largest source of AABW, has experienced the largest freshening. Here we use 23 years of summer measurements to document temporal variability in the salinity of the Ross Sea High Salinity Shelf Water (HSSW), a precursor to RSBW. HSSW salinity decreased between 1995 and 2014, consistent with freshening observed between 1958 and 2008. However, HSSW salinity rebounded sharply after 2014, with values in 2018 similar to those observed in the mid-late 1990s. Near-synchronous interannual fluctuations in salinity observed at five locations on the continental shelf suggest that upstream preconditioning and large-scale forcing influence HSSW salinity. The rate, magnitude and duration of the recent salinity increase are unusual in the context of the (sparse) observational record. 

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. 

Marine microeukaryotes play a fundamental role in biogeochemical cycling through the transfer of energy to higher trophic levels and vertical carbon transport. Despite their global importance, microeukaryote physiology, nutrient metabolism and contributions to carbon cycling across offshore ecosystems are poorly characterized. Here, we observed the prevalence of dinoflagellates along a 4,600-km meridional transect extending across the central Pacific Ocean, where oligotrophic gyres meet equatorial upwelling waters rich in macronutrients yet low in dissolved iron. A combined multi-omics and geochemical analysis provided a window into dinoflagellate metabolism across the transect, indicating a continuous taxonomic dinoflagellate community that shifted its functional transcriptome and proteome as it extended from the euphotic to the mesopelagic zone. In euphotic waters, multi-omics data suggested that a combination of trophic modes were utilized, while mesopelagic metabolism was marked by cytoskeletal investments and nutrient recycling. Rearrangement in nutrient metabolism was evident in response to variable nitrogen and iron regimes across the gradient, with no associated change in community assemblage. Total dinoflagellate proteins scaled with particulate carbon export, with both elevated in equatorial waters, suggesting a link between dinoflagellate abundance and total carbon flux. Dinoflagellates employ numerous metabolic strategies that enable broad occupation of central Pacific ecosystems and play a dual role in carbon transformation through both photosynthetic fixation in the euphotic zone and remineralization in the mesopelagic zone. 

Emiliania huxleyi is a bloom-forming microalga that affects the global sulfur cycle by producing large amounts of dimethylsulfoniopropionate (DMSP) and its volatile metabolic product dimethyl sulfide. Top-down regulation of E. huxleyi blooms has been attributed to viruses and grazers; however, the possible involvement of algicidal bacteria in bloom demise has remained elusive. We demonstrate that a Roseobacter strain, Sulfitobacter D7, that we isolated from a North Atlantic E. huxleyi bloom, exhibited algicidal effects against E. huxleyi upon coculturing. Both the alga and the bacterium were found to co-occur during a natural E. huxleyi bloom, therefore establishing this host-pathogen system as an attractive, ecologically relevant model for studying algal-bacterial interactions in the oceans. During interaction, Sulfitobacter D7 consumed and metabolized algal DMSP to produce high amounts of methanethiol, an alternative product of DMSP catabolism. We revealed a unique strain-specific response, in which E. huxleyi strains that exuded higher amounts of DMSP were more susceptible to Sulfitobacter D7 infection. Intriguingly, exogenous application of DMSP enhanced bacterial virulence and induced susceptibility in an algal strain typically resistant to the bacterial pathogen. This enhanced virulence was highly specific to DMSP compared to addition of propionate and glycerol which had no effect on bacterial virulence. We propose a novel function for DMSP, in addition to its central role in mutualistic interactions among marine organisms, as a mediator of bacterial virulence that may regulate E. huxleyi blooms. 

Abstract. Phaeocystis antarctica is an important phytoplankter of the Ross Sea where it dominates the early season bloom after sea ice retreat and is a major contributor to carbon export. The factors that influence Phaeocystis colony formation and the resultant Ross Sea bloom initiation have been of great scientific interest, yet there is little known about the underlying mechanisms responsible for these phenomena. Here, we present laboratory and field studies on Phaeocystis antarctica grown under multiple iron conditions using a coupled proteomic and transcriptomic approach. P. antarctica had a lower iron limitation threshold than a Ross Sea diatom Chaetoceros sp., and at increased iron nutrition (&gt;120pM Fe') a shift from flagellate cells to a majority of colonial cells in P. antarctica was observed, implying a role for iron as a trigger for colony formation. Proteome analysis revealed an extensive and coordinated shift in proteome structure linked to iron availability and life cycle transitions with 327 and 436 proteins measured as significantly different between low and high iron in strains 1871 and 1374, respectively. The enzymes flavodoxin and plastocyanin that can functionally replace iron metalloenzymes were observed at low iron treatments consistent with cellular iron-sparing strategies, with plastocyanin having a larger dynamic range. The numerous isoforms of the putative iron-starvation-induced protein (ISIP) group (ISIP2A and ISIP3) had abundance patterns coinciding with that of either low or high iron (and coincident flagellate or the colonial cell types in strain 1871), implying that there may be specific iron acquisition systems for each life cycle type. The proteome analysis also revealed numerous structural proteins associated with each cell type: within flagellate cells actin and tubulin from flagella and haptonema structures as well as a suite of calcium-binding proteins with EF domains were observed. In the colony-dominated samples a variety of structural proteins were observed that are also often found in multicellular organisms including spondins, lectins, fibrillins, and glycoproteins with von Willebrand domains. A large number of proteins of unknown function were identified that became abundant at either high or low iron availability. These results were compared to the first metaproteomic analysis of a Ross Sea Phaeocystis bloom to connect the mechanistic information to the in situ ecology and biogeochemistry. Proteins associated with both flagellate and colonial cells were observed in the bloom sample consistent with the need for both cell types within a growing bloom. Bacterial iron storage and B₁₂ biosynthesis proteins were also observed consistent with chemical synergies within the colony microbiome to cope with the biogeochemical conditions. Together these responses reveal a complex, highly coordinated effort by P. antarctica to regulate its phenotype at the molecular level in response to iron and provide a window into the biology, ecology, and biogeochemistry of this group. 

Environmental contextCobalamin, or vitamin B12, is receiving increased attention as a critical trace nutrient in the growth and metabolic processes of oceanic phytoplankton and bacterial communities. We present evidence that indicates B12 has a more significant role in the biogeochemical cycling of the climatically important compounds dimethylsulfide and dimethylsulfoniopropionate than previously understood. Several possible mechanisms are examined that link cellular-level processes involving B12 to global-scale biogeochemical processes involving the oceanic cycling of dimethylsulfoniopropionate and dimethylsulfide.AbstractEvidence is presented showing that dissolved dimethylsulfoniopropionate (DMSPd) and dimethylsulfide (DMS) concentrations are influenced by the availability of vitamin B12 in two oceanographically distinct regions with different DMS production capacities, the central equatorial Pacific Ocean and the Ross Sea, Antarctica. In both locations, addition of B12 to incubation experiments resulted in decreases in DMS and, in some cases, DMSPd concentrations relative to unamended controls. In no case did increasing iron availability significantly (α=0.1) alter DMS concentrations relative to controls. The relative decreases in DMS between B12 addition and control experiments were significant (α=0.1) in five of seven experiments conducted at ambient iron levels. Overall, DMS concentrations were on average 33.4% (±15.1%; 1 standard deviation) lower, relative to unamended controls, by the end of incubation experiments when B12 was added. Declines in DMSPd were observed in three of five experiments. Similar trends were observed when B12 was added to iron-supplemented bottle incubation experiments (30.4±10.4% lower final DMS concentrations in +B12Fe treatments relative to +Fe treatments). Several possible molecular-level explanations exist for this link between B12 and DMS production, including potential B12 dependence of methyltransferase enzymes involved in both DMS and DMSP degradation. Although the enzymology of these reactions remains unclear, the relationships described here provide evidence for plausible mechanisms behind the microbial modulation of oceanic DMS. 

Environmental contextDimethylsulfoniopropionate (DMSP), a small sulfur compound biosynthesised by algae, plays an important role in global climate, particularly in polar regions. We investigated salinity effects on DMSP levels, and provide the first experimental measurements of DMSP and associated physiological changes in a polar diatom across to a range of gradual salinity shifts representative of sea-ice conditions. Quantitative estimates of DMSP in polar diatoms following salinity changes will facilitate new mathematical models to predict seasonal responses and reactions to climate change.AbstractAlthough extreme environmental gradients within sea-ice have been proposed to stimulate dimethylsulfoniopropionate (DMSP) accumulation in diatoms, a taxa whose temperate counterparts show relatively low concentrations, this has yet to be experimentally validated across a range of salinities representative of sea-ice conditions. The present study examined changes in DMSP concentrations in the widespread polar diatom Fragilariopsis cylindrus in response to gradual salinity shifts representative of those encountered during sea-ice formation and melt. DMSP concentrations were elevated up to 127% in 70-salinity cultures. Low-salinity shifts decreased intracellular DMSP concentrations in a gradient-dependent manner that suggests DMSP recycling rather than release under milder hyposalinity shifts. Permeable membranes were detected in ~45% of 10-salinity cells; therefore, loss of membrane integrity may only partially explain DMSP release in the lowest-salinity group. Growth rates, photosynthetic efficiency of photosystem II and reactive oxygen species detection indicated only partial impairment by salinity stress in this organism. Thus, experimental evidence supports the role of DMSP as a compatible solute in the acclimation of a sea-ice diatom across large salinity gradients and measurements of associated physiological changes will improve interpretation of environmental measurements.