Unravelling Metal Speciation in the Microenvironment Surrounding Phytoplankton Cells to Improve Predictions of Metal Bioavailability.

Fengjie Liu,Dominik Weiss,Claude Fortin,Anne Crémazy,Peter G C Campbell,Qiao-Guo Tan

doi:10.1021/acs.est.9b07773

Abstract

A lack of knowledge on metal speciation in the microenvironment surrounding phytoplankton cells (i.e., the phycosphere) represents an impediment to accurately predicting metal bioavailability. Phycosphere pH and O2 concentrations from a diversity of algae species were compiled. For marine algae in the light, the average increases were 0.32 pH units and 0.17 mM O2 in the phycosphere, whereas in the dark the average decreases were 0.10 pH units and 0.03 mM O2, in comparison to bulk seawater. In freshwater algae, the phycosphere pH increased by 1.28 units, whereas O2 increased by 0.38 mM in the light. Equilibrium modeling showed that the pH alteration influenced the chemical species distribution (i.e., free ion, inorganic complexes, and organic complexes) of Al, Cd, Co, Cu, Fe, Hg, Mn, Ni, Pb, Sc, Sm, and Zn in the phycosphere, and the O2 fluctuation increased oxidation rates of Cu(I), Fe(II) and Mn(II) from 2 to 938-fold. The pH/O2-induced changes in phycosphere metal chemistry were larger for freshwater algae than for marine species. Reanalyses of algal metal uptake data in the literature showed that uptake of the trivalent metals (Sc, Sm and Fe), in addition to divalent metals, can be better predicted after considering the phycosphere chemistry.

Highlights

Microscopic plant-like organisms called phytoplankton carry out more than 50% of global CO2 fixation,[1] and their growth is influenced by the availability of micronutrient metals such as Fe, Cu, Zn, Co, and Mn in many aquatic ecosystems, especially the oceans.[2]
Several studies consistently show that key chemical conditions such as pH and O2 concentrations in the phycosphere significantly differed from those in bulk waters.[8−10] For example, when a marine diatom was exposed to light, the phycosphere pH increased up to 0.9 units and the phycosphere O2 concentration doubled.[9]
An example of the calculation of Cu complexation kinetic by dissolved organic carbon (DOC) in the phycosphere is given in the Supporting Information (SI) (Note S3), and the results suggested that Cu equilibrated with DOC in this thin layer

Summary

■ INTRODUCTION

Microscopic plant-like organisms called phytoplankton carry out more than 50% of global CO2 fixation,[1] and their growth is influenced by the availability of micronutrient metals such as Fe, Cu, Zn, Co, and Mn in many aquatic ecosystems, especially the oceans.[2]. Article calculated within the observed phycosphere pH range, and speciation in bulk waters was calculated for comparison Among these three metal groups, the free metal ion is considered as the best predictor of metal bioavailability,[6] inorganic complexes of some metals such as Fe have been shown to contribute to metal uptake by some phytoplankton species.[36,37] Alternatively, metals complexed by DOC generally cannot be directly assimilated by algal cells.[38]. A number of “unexpected” results of metal uptake (i.e., significant derivation from the uptake rates predicted on the basis of the free metal ion concentration in the bulk solution) have been reported, even in chemically well-defined media These puzzling data include both divalent metals (e.g., Cd, Zn, Cu, and Pb)[12,14,15,46−49] and trivalent ones (e.g., rare earth metals and Fe),[50−55] in the presence of either synthetic or natural ligands.

■ RESULTS AND DISCUSSION

■ ACKNOWLEDGMENTS

■ REFERENCES