Isotopic evidence for nickel limitation of biological productivity in the ocean

Abstract

Abstract Nickel (Ni) is an essential element for many important enzyme systems 1,2 . Two puzzling aspects of Ni biogeochemical cycling in the modern ocean have emerged. First, unlike a number of bio-essential elements, Ni is never fully depleted in the surface ocean 3-13 . Second, a heavy Ni isotopic composition in the surface ocean, indicative of removal of light isotopes likely by productivity, is not observed globally 6-13 . Active debate persists regarding the isotopic fractionation of Ni associated with biological uptake and the bioavailability of Ni in the ocean 7,9,11-13 . Here we show that, in contrast to biological isotopic fractionation for most other elements, three cosmopolitan phytoplankton species preferentially take up isotopically heavy Ni from the culture media, with species-dependent magnitudes of fractionation, under varying Ni availability. This fractionation towards heavy Ni isotopes can be explained, in our experiments, by the characteristic strong Ni-binding of cellular metal acquisition systems, relative to weaker binding by ligands in the culture media, with a secondary influence of cellular relocation and/or efflux. In the open ocean, an inferred stronger binding of Ni to ligands present in seawater, relative to that of the phytoplankton, yields the inverse fractionation (towards light isotopes in the biomass) and limits the bioavailability of metals in the surface ocean. Reconciling seawater Ni concentration and isotope data, results from incubation experiments, and marine gene biogeography, we demonstrate that Ni is limited for marine phytoplankton in the mid-latitude surface ocean with low Ni concentration and heavy Ni isotope composition, with implications for the significance of Ni bioavailability on both ocean productivity and carbon cycling.