The Ni cycle in the Southern Ocean: insights from Ni concentrations, isotopes and metagenomics

Nickel (Ni) is an essential micronutrient for marine microorganisms, involved in enzymes controlling the nitrogen cycle and metabolic responses to oxidative stress. In this study, we examine the role of potential Ni utilisation by marine microorganisms in oceanic Ni and δ60Ni distributions, and specifically the influence of Ni-containing enzyme abundances on Ni isotope fractionation. Dissolved Ni concentrations and isotope compositions were measured together with microbial gene composition in Southern Ocean samples from the Antarctic Circumnavigation Expedition. We show that lower Ni concentrations are associated with higher δ60Ni values in surface waters north of the Sub-Antarctic Front compared to southerly locations. The high-latitude Mertz Glacier stands as an exception, as systematics between Ni and δ60Ni resemble those of low-latitude stations. No single enzyme could be identified as the sole driver of δ60Ni variations across all stations, as the strength and significance of correlations varied depending on the level of precision of functional annotations and the size fractions considered. Still, relative abundances of gene clusters annotated as urease and Ni superoxide dismutase (Ni-SOD) enzymes in metagenomes correlated with δ60Ni, suggesting the preferential removal of isotopically light Ni by microorganisms using these enzymes. Despite differences in enzymatic and taxonomic profiles, the three stations exhibiting heavy surface Ni isotope compositions share a specific nitrogen biogeochemistry, characterised by high particulate organic nitrogen pool and strong nitrate consumption. We thus hypothesise that Ni and δ60Ni distributions reflect variations in Ni metabolic requirements driven by complex microbial and enzymatic activity linked to the relative availability of inorganic and organic nitrogen. We further propose that the use of urea as an alternative nitrogen source during the late productive season could explain the unexpected isotope fractionation observed at Mertz. This study represents an initial exploration of the influence of enzymes and microbial communities on the Ni biogeochemical divide.