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Abstract The North Pacific subtropical gyre is a globally important contributor to carbon uptake despite being a persistently oligotrophic ecosystem. Supply of the micronutrient iron to the upper ocean varies seasonally to episodically, and when coupled with rapid biological consumption, results in low iron concentrations. In this study, we examined changes in iron uptake rates, along with siderophore concentrations and biosynthesis potential at Station ALOHA across time (2013–2016) and depth (surface to 500 m) to observe changes in iron acquisition and internal cycling by the microbial community. The genetic potential for siderophore biosynthesis was widespread throughout the upper water column, and biosynthetic gene clusters peaked in spring and summer along with siderophore concentrations, suggesting changes in nutrient delivery, primary production, and carbon export seasonally impact iron acquisition. Dissolved iron turnover times, calculated from iron‐amended experiments in surface (15 m) and mesopelagic (300 m) waters, ranged from 9 to 252 d. The shortest average turnover times at both depths were associated with inorganic iron additions (14  9 d) and the longest with iron bound to strong siderophores (148  225 d). Uptake rates of siderophore‐bound iron were faster in mesopelagic waters than in the surface, leading to high Fe : C uptake ratios of heterotrophic bacteria in the upper mesopelagic. The rapid cycling and high demand for iron at 300 m suggest differences in microbial metabolism and iron acquisition in the mesopelagic compared to surface waters. Together, changes in siderophore production and consumption over the seasonal cycle suggest organic carbon availability impacts iron cycling at Station ALOHA. 

Iodine intersects with the marine biogeochemical cycles of several major elements and can influence air quality through reactions with tropospheric ozone. Iodine is also an element of interest in paleoclimatology, whereby iodine-to-calcium ratios in marine carbonates are widely used as a proxy for past ocean redox state. While inorganic iodine in seawater is found predominantly in its reduced and oxidized anionic forms, iodide (I⁻) and iodate (IO₃⁻), the rates, mechanisms and intermediate species by which iodine cycles between these inorganic pools are poorly understood. Here, we address these issues by characterizing the speciation, composition and cycling of iodine in the upper 1,000 m of the water column at Station ALOHA in the subtropical North Pacific Ocean. We first obtained high-precision profiles of iodine speciation using isotope dilution and anion exchange chromatography, with measurements performed using inductively coupled plasma mass spectrometry (ICP-MS). These profiles indicate an apparent iodine deficit in surface waters approaching 8% of the predicted total, which we ascribe partly to the existence of dissolved organic iodine that is not resolved during chromatography. To test this, we passed large volumes of seawater through solid phase extraction columns and analyzed the eluent using high-performance liquid chromatography ICP-MS. These analyses reveal a significant pool of dissolved organic iodine in open ocean seawater, the concentration and complexity of which diminish with increasing water depth. Finally, we analyzed the rates of IO₃⁻formation using shipboard incubations of surface seawater amended with¹²⁹I⁻. These experiments suggest that intermediate iodine species oxidize to IO₃⁻much faster than I⁻does, and that rates of IO₃⁻formation are dependent on the presence of particles, but not light levels. Our study documents the dynamics of iodine cycling in the subtropical ocean, highlighting the critical role of intermediates in mediating redox transformations between the major inorganic iodine species. 

Phosphonates are organophosphorus metabolites with a characteristic C-P bond. They are ubiquitous in the marine environment, their degradation broadly supports ecosystem productivity, and they are key components of the marine phosphorus (P) cycle. However, the microbial producers that sustain the large oceanic inventory of phosphonates as well as the physiological and ecological roles of phosphonates are enigmatic. Here, we show that phosphonate synthesis genes are rare but widely distributed among diverse bacteria and archaea, including Prochlorococcus and SAR11, the two major groups of bacteria in the ocean. In addition, we show that Prochlorococcus can allocate over 40% of its total cellular P-quota toward phosphonate production. However, we find no evidence that Prochlorococcus uses phosphonates for surplus P storage, and nearly all producer genomes lack the genes necessary to degrade and assimilate phosphonates. Instead, we postulate that phosphonates are associated with cell-surface glycoproteins, suggesting that phosphonates mediate ecological interactions between the cell and its surrounding environment. Our findings indicate that the oligotrophic surface ocean phosphonate pool is sustained by a relatively small fraction of the bacterioplankton cells allocating a significant portion of their P quotas toward secondary metabolism and away from growth and reproduction. 

Metabolites that incorporate elements other than carbon, nitrogen, hydrogen and oxygen can be selectively detected by inductively coupled mass spectrometry (ICPMS). When used in parallel with chromatographic separations and conventional electrospray ionization mass spectrometry (ESIMS), ICPMS allows the analyst to quickly find, characterize and identify target metabolites that carry nutrient elements (P, S, trace metals; “nutrient metabolites”), which are of particular interest to investigations of microbial biogeochemical cycles. This approach has been applied to the study of siderophores and other trace metal organic ligands in the ocean. The original method used mass search algorithms that relied on the ratio of stable isotopologues of iron, copper and nickel to assign mass spectra collected by ESIMS to metabolites carrying these elements detected by ICPMS. However, while isotopologue-based mass assignment algorithms were highly successful in characterizing metabolites that incorporate some trace metals, they do not realize the whole potential of the ICPMS/ESIMS approach as they cannot be used to assign the molecular ions of metabolites with monoisotopic elements or elements for which the ratio of stable isotopes is not known. Here we report a revised ICPMS/ESIMS method that incorporates a number of changes to the configuration of instrument hardware that improves sensitivity of the method by a factor of 4–5, and allows for more accurate quantitation of metabolites. We also describe a new suite of mass search algorithms that can find and characterize metabolites that carry monoisotopic elements. We used the new method to identify siderophores in a laboratory culture of Vibrio cyclitrophicus and a seawater sample collected in the North Pacific Ocean, and to assign molecular ions to monoisotopic cobalt and iodine nutrient metabolites in extracts of a laboratory culture of the marine cyanobacterium Prochorococcus MIT9215. 

Abstract In the oligotrophic ocean where inorganic phosphate (P_i) concentrations are low, microorganisms supplement their nutrient requirements with phosphorus (P) extracted from dissolved organic matter (DOM). Most P in DOM is bound as phosphate esters, which are hydrolyzed by phosphoesterases to P_i. However, a large fraction of DOM‐P occurs as phosphonates, reduced organophosphorus compounds with a CP bond that do not yield P_ithrough simple ester hydrolysis alone. Phosphonates require an additional step that cleaves the CP bond and oxidizes P(III) to P(V) to yield P_i. Most phosphonates are metabolized by the C‐P lyase pathway, which cleaves CP bonds and oxidizes phosphonates to P_i, enabling microbial assimilation. While the activity of common phosphoesterases such as alkaline phosphatase and phosphodiesterase can be measured by a fluorescent assay, a comparable method to assess C‐P lyase activity (CLA) in natural water samples does not exist. To address this, we synthesized a dansyl‐labeled phosphonate compound, and measured its hydrolysis by C‐P lyase using high performance liquid chromatography. We found that laboratory cultures of marine bacteria expressing the C‐P lyase pathway are able to hydrolyze the dansyl phosphonate, while bacteria expressing other phosphonate degradation pathways do not. Finally, we performed several field tests of the assay to measure water column profiles of CLA at Sta. ALOHA in the North Pacific Subtropical Gyre. Activity was elevated near the deep chlorophyll maximum suggesting high levels of phosphonate degradation in that region. 

Abstract In oligotrophic ocean regions, dissolved organic phosphorus (DOP) plays a prominent role as a source of phosphorus (P) to microorganisms. An important bioavailable component of DOP is phosphonates, organophosphorus compounds with a carbon‐phosphorus (C‐P) bond, which are ubiquitous in high molecular weight dissolved organic matter (HMWDOM). In addition to being a source of P, the degradation of phosphonates by the bacterial C‐P lyase enzymatic pathway causes the release of trace hydrocarbon gases relevant to climate and atmospheric chemistry. In this study, we investigated the roles of phosphate and phosphonate cycling in the production of methane (CH₄) and ethylene (C₂H₄) in the western North Atlantic Ocean, a region that features a transition in phosphate concentrations from coastal to open ocean waters. We observed an inverse relationship between phosphate and the saturation state of CH₄and C₂H₄in the water column, and between phosphate and the relative abundance of the C‐P lyase marker genephnJ. In phosphate‐depleted waters, methylphosphonate and 2‐hydroxyethylphosphonate, the C‐P lyase substrates that yield CH₄and C₂H₄, respectively, were readily degraded in proportions consistent with their abundance and bioavailability in HMWDOM and with the concentrations of CH₄and C₂H₄in the water column. We conclude that phosphonate degradation through the C‐P lyase pathway is an important source and a common production pathway of CH₄and C₂H₄in the phosphate‐depleted surface waters of the western North Atlantic Ocean and that phosphate concentration can be an important control on the saturation state of these gases in the upper ocean. 

Abstract Coastal upwelling of nutrients and metals along eastern boundary currents fuels some of the most biologically productive marine ecosystems. Although iron is a main driver of productivity in many of these regions, iron cycling and acquisition by microbes remain poorly constrained, in part due to the unknown composition of organic ligands that keep bioavailable iron in solution. In this study, we investigated organic ligand composition in discrete water samples collected across the highly productive California Coastal upwelling system. Siderophores were observed in distinct nutrient regimes at concentrations ranging from 1 pM to 18 pM. Near the shallow continental shelf, ferrioxamine B was observed in recently upwelled, high chlorophyll surface waters while synechobactins were identified within nepheloid layers at 60–90 m depth. In offshore waters characterized by intermediate chlorophyll, iron, and nitrate concentrations, we found amphibactins and an unknown siderophore with a molecular formula of C₃₃H₅₈O₈N₅Fe. Highest concentrations were measured in the photic zone, however, amphibactins were also found in waters as deep as 1500 m. The distribution of siderophores provides evidence for microbial iron deficiency across a range of nutrient regimes and indicates siderophore production and acquisition is an important strategy for biological iron uptake in iron limited coastal systems. Polydisperse humic ligands were also detected throughout the water column and were particularly abundant near the benthic boundary. Our results highlight the fine‐scale spatial heterogeneity of metal ligand composition in an upwelling environment and elucidate distinct sources that include biological production and the degradation of organic matter in suboxic waters.