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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.

We present a new approach for quantifying the bioavailability of dissolved iron (dFe) to oceanic phytoplankton. Bioavailability is defined using an uptake rate constant (k_in‐app) computed by combining data on: (a) Fe content of individual in situ phytoplankton cells; (b) concurrently determined seawater dFe concentrations; and (c) growth rates estimated from the PISCES model. We examined 930 phytoplankton cells, collected between 2002 and 2016 from 45 surface stations during 11 research cruises. This approach is only valid for cells that have upregulated their high‐affinity Fe uptake system, so data were screened, yielding 560 single cellk_in‐appvalues from 31 low‐Fe stations. We normalizedk_in‐appto cell surface area (S.A.) to account for cell‐size differences.

The resulting bioavailability proxy (k_in‐app/S.A.) varies among cells, but all values are within bioavailability limits predicted from defined Fe complexes. In situ dFe bioavailability is higher than model Fe‐siderophore complexes and often approaches that of highly available inorganic Fe′. Station averagedk_in‐app/S.A. are also variable but show no systematic changes across location, temperature, dFe, and phytoplankton taxa. Given the relative consistency ofk_in‐app/S.A. among stations (ca. five‐fold variation), we computed a grand‐averaged dFe availability, which upon normalization to cell carbon (C) yieldsk_in‐app/C of 42,200 ± 11,000 L mol C⁻¹ d⁻¹. We utilizek_in‐app/C to calculate dFe uptake rates and residence times in low Fe oceanic regions. Finally, we demonstrate the applicability ofk_in‐app/C for constraining Fe uptake rates in earth system models, such as those predicting climate mediated changes in net primary production in the Fe‐limited Equatorial Pacific.

Phytoplankton iron contents (i.e., quotas) directly link biogeochemical cycles of iron and carbon and drive patterns of nutrient limitation, recycling, and export. Ocean biogeochemical models typically assume that iron quotas are either static or controlled by dissolved iron availability. We measured iron quotas in phytoplankton communities across nutrient gradients in the Pacific Ocean and found that quotas diverged significantly in taxon‐specific ways from laboratory‐derived predictions. Iron quotas varied 40‐fold across nutrient gradients, and nitrogen‐limitation allowed diatoms to accumulate fivefold more iron than co‐occurring flagellates even under low iron availability. Modeling indicates such “luxury” uptake is common in large regions of the low‐iron Pacific Ocean. Among diatoms, both pennate and centric genera accumulated luxury iron, but the cosmopolitan pennate genusPseudo‐nitzschiamaintained iron quotas 10‐fold higher than co‐occurring centric diatoms, likely due to enhanced iron storage. Biogeochemical models should account for taxonomic and macronutrient controls on phytoplankton iron quotas.