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

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 O 2 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 O 2 in the phycosphere, whereas in the dark the average decreases were 0.10 pH units and 0.03 mM O 2 , in comparison to bulk seawater. In freshwater algae, the phycosphere pH increased by 1.28 units, whereas O 2 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 O 2 fluctuation increased oxidation rates of Cu(I), Fe(II) and Mn(II) from 2 to 938-fold. The pH/O 2 -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.

Synergistic use of siderophores and weak organic ligands during zinc transport in the rhizosphere controlled by pH and ion strength gradients

“…Siderophores can have a distinct non-classical function to take up metals other than Fe and play an important role as zincophores in rice soils. In line with recent findings 3 , 24 , 30 , 34 , 36 , 43 , 72 , the present study supports the conclusion that siderophores are central to access Zn in the soil.…”

“…After the formation of a labile complex at the mineral surface, a ligand exchange reaction takes place in which the metal is transferred to a ligand with high Fe affinity and the low affinity ligand is free to react with the mineral again. Modelling and experimental studies of organic ligand complexation with a wide range of first row transition metals have demonstrated that pH and ionic strength exert a critical influence on the stability and lability of metal–ligand complexes 3 , 21 – 24 . The rhizosphere indeed is characterised by microscale gradients in pH and ionic strength, so it is reasonable to expect that these two master variables play a central part in synergistic roles of siderophores and other organic ligands during mobilisation and transport of zinc in the rhizosphere.…”

Exploiting Catabolite Repression and Stringent Response to Control Delay and Multimodality of Bioluminescence Signal by Metal Whole-Cell Biosensors: Interplay between Metal Bioavailability and Nutritional Medium Conditions

“…Difficulties include the proper evaluation of the interplay between the (i) bioavailability features of the metal species in the extracellular medium [10][11][12], (ii) metal biouptake flux at the biosensor surface, and (iii) kinetics of the intracellular biochemical reactions leading to photons emission [13,14]. In particular, items (i) and (ii) depend on the dynamics of metal ion speciation defined by the pertaining rate parameters for the formation and dissociation of metal complexes involving ionic, molecular and/or particulate metal ligands dispersed in solution [12,15,16]. In turn, these rate constants, together with the diffusion properties of the various metal forms, determine the lability of the complexed metal species, i.e., their contribution to the dynamic supply of free metals to the biosensor surface [12,15].…”

Phycosphere pH of unicellular nano- and micro- phytoplankton cells and consequences for iron speciation

“…Precise quantification of chemical conditions in the phycosphere is crucial for better understanding how phytoplankton will respond to environmental changes. Evidence is emerging that interactions between phytoplankton and abiotic/biotic environments are governed by micro-and nano-scale interfacial processes [13,47,49,50], which cannot be determined using bulk water analyses. Small changes in the phycosphere likely translate into large impacts on the oceanic carbon and nitrogen cycle (Fig.…”

“…Ocean acidification will also affect calcium carbonate production and may drive distinct malformations of coccolith structures for calcifying phytoplankton species [9]. However, pH conditions in the micro-scale region surrounding phytoplankton cells can differ markedly from ambient bulk seawater, as observed in giant diatoms and algal colonies [10][11][12][13]. The microenvironment, known as the phycosphere [14], is the unstirred boundary layer in the immediate vicinity of an algal cell, where the effects of algal metabolisms and other associated microorganisms can be significant.…”