Within APPELS, we have been able to elucidate a role for trace metals in controlling the growth and distribution of different microbes that mediate the supply of nitrogen for the biological pump:
1) We have investigated the Fe requirements and Fe uptake strategies of the Nitrosopumilus maritimus strain SCM1, a strain representative of globally abundant marine AOA. N. maritimus growth may be Fe limited due to its highest iron requirement of all marine microbes (Shafiee et al., 2019). Nitrosopumilus maritimus strain SCM1 (AOA) and Nitrosococcus oceani strain C-107 (AOB) have contrasting physiologies in response to the trace metals iron (Fe) and copper (Cu). We propose the testable hypothesis that ammonia oxidation is limited by Cu in large tracts of the open ocean and suggest a relatively earlier emergence of AOB than AOA when considered in the context of evolving trace metal availabilities over geologic time (Shafiee et al., 2021).
The differential response of algae to limiting and toxic levels of metals reveals contrasting metal management systems which explain both their global distribution and the phytoplankton succession during the geological past:
2) The different responses to Cr exposure reveal contrasting strategies for metal uptake and homeostasis in algal lineages. At high Cr(VI) concentrations, red lineages experience growth inhibition through reduced photosynthetic capability, while green lineages are completely unaffected. Green algae have higher specificity transporters to prevent Cr(VI) from entering the cell, and more specific intracellular stores of Cr within the membrane fraction than the red algae, which accumulate more Cr mistakenly in the cytosol fraction via lower affinity transport mechanisms (Wilson et al., 2019). Green algal approaches require greater nutrient investments in the more numerous transport proteins required and management of specific metals, a strategy better adapted to the resource-rich coastal waters. By contrast the red algae are nutrient efficient with fewer and less discriminate metal transporters which can be fast and better adapted in the oligotrophic, oxygenated open ocean which has prevailed since the deepening of the oxygen minimum zones at the start of the Mesozoic (Zhang et al., 2022).
The Ni isotopic fractionation by phytoplankton shows a totally new conceptual understanding of biological metal isotopic fractionation:
3) We have shown that, in contrast to biological isotopic fractionation for 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 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. We demonstrate that Ni is limited for marine phytoplankton in the mid-latitude surface ocean with low Ni concentration and heavy Ni isotope composition (Wang et al., in review Nature Geoscience).
