Coupling macro- and micronutrient biogeochemistry: distribution and speciation of iron and other bioactive trace metals required for phosphorus acquisition in the subtropical North Atlantic

Abstract

To meet cellular phosphorus (P) demands in the phosphate-deplete subtropical North Atlantic, phytoplankton depend on the less readily bioavailable dissolved organic phosphorus (DOP), which is accessible via alkaline phosphatases – metalloenzymes that require co-factors of iron (Fe), zinc(Zn) or cobalt (Co). As the oceanic concentrations of these metals are vanishingly low and as their physicochemical speciation further constrains bioavailability, the coupled biogeochemistry of macronutrient P and metal micronutrients Fe, Zn and Co has the potential to exert a biological control on primary production and hence, impact upon the global carbon cycle. A summertime longitudinal transect along 22 °N between 60 °W to 30 °W in the subtropical North Atlantic gyre served as a natural laboratory for this thesis, to investigate the distribution, speciation and biological control of Fe (and Zn and Co) for DOP acquisition across strong biogeochemical gradients in metals, macronutrients and phytoplankton community. High-resolution surface sampling and full-depth water column profiling of the Fe distribution were conducted and size-fractionated into soluble (sFe <0.02 µm), colloidal (0.02 µm unfiltered, acid-leachable) Fe species, which revealed the pervasive role of cFe in driving the distribution of dissolved Fe (dFe <0.2 µm, i.e. dFe = cFe + sFe). While the largest local input across the basin was due to hydrothermal venting from the Mid-Atlantic ridge in the abyss, where dFe reached 27 nM with ~90 % cFe, the surface dFe inventory was strongly controlled by seasonal dust deposition. This resulted in a strong west-to-east decrease in dFe concentrations from 1.53 to 0.26nM, with the colloidal fraction decreasing concurrently (from 85 to 61 % of dFe). Particle scavenging and biological uptake were the major removal processes of dFe and cFe in the subsurface, drawing cFe down to 0 to 30 % of dFe in the deep chlorophyll-a maximum (DCM). Due the pivotal position of cFe between the particulate and the soluble (i.e. the truly dissolved) phases, it was responsible for setting the dFe inventory at the major sources and sinks across the basin. Building on these insights, at three representative locations that differed in dust loading and initial Fe concentrations, kinetics bottle experiments were carried out, in which Fe additions enriched in the low abundance isotope 57Fe (as dissolved Fe2O3, i.e. inorganic sFe) were made to ambient surface seawater to trace the partitioning into the sFe, cFe and TDFe pools over a 48 h incubation period. Due to the low solubility of Fe in seawater and the absence of excess organic ligands, the 57Feenriched spike partitioned rapidly (<30 min), almost completely (~90 %), consistently (regardless of initial conditions) and irreversibly (unchanged over 48 h) into the colloidal phase, as nanoparticulate Fe-oxyhydroxides. As these are precursors to larger mineral phases, which remove available dFe and reduce its residence time in surface waters, this result strengthens the argument for the important role of cFe in the oceanic Fe cycle. The cross-basin gradients in surface Fe concentration and speciation, and less variable dZn and dCo distributions, enabled in-situ bioassays with metal amendments to probe the effects of trace metals on DOP acquisition. Calibrated targeted proteomics were applied to quantify the alkaline phosphatases of dominant phytoplankton species, and demonstrated the localised effect of metal availability on alkaline phosphatase abundances at two out of four locations. In the high Fe, low DIP, low DOP western basin, additions of Zn and Co increased the concentration of a Zn/Co-dependent PhoA-type alkaline phosphatase of Synechococcus six- and seven-fold, respectively, relative to the unamended Control. In the lower Fe, higher DIP, higher DOP eastern basin, the addition of Fe increased the concentration of the Fe-dependent PhoX of Prochlorococcus two-fold relative to the Control. Using cellular metal stoichiometry in Synechococcus revealed PhoA to be a potential major sink for cellular Co (1 to 35 %), but not Zn (<1 %), and hence, it may be particularly sensitive to Co availability globally. Biogeochemical gradients are considered characteristic of latitudinal progression across basins, e.g. from the high Fe North Atlantic into the low Fe South Atlantic. There is, however, a systematic lack of knowledge across longitudinal gradients and therefore, their biogeochemical impact may be underestimated. The key findings of this thesis demonstrate that the biogeochemistry within the subtropical North Atlantic is diverse, as ) the Fe distribution is subject to large regional variability that is controlled by a dynamic colloidal phase, and ) metal availability affects P acquisition locally. The combined toolbox of traditional biogeochemical measurements, trace metal measurements, and proteomics was essential to these results, and will prove inevitable in constraining their implications in the future, especially as global change is predicted to alter metal cycles and exacerbate P stress.

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Identifiers

ORCID for Maeve Lohan: orcid.org/0000-0002-5340-3108

ORCID for Christopher Moore: orcid.org/0000-0002-9541-6046

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