THE INFLUENCE OF pH ON ALGAL CELL MEMBRANE PERMEABILITY AND ITS IMPLICATIONS FOR THE UPTAKE OF LIPOPHILIC METAL COMPLEXES¹

Abstract

Uptake of lipophilic metal complexes by freshwater algae has recently been shown to be pH dependent. Here we look at different physiological aspects that could influence the diffusion of the lipophilic Cd complex, Cd(diethyldithiocarbamate)2 (0) (Cd(DDC)2 (0) ), into algal cells at different exposure pH values. Changes in cell membrane permeability were assessed as a function of pH for three species of green algae [Chlamydomonas reinhardtii P. A. Dang., Pseudokirchneriella subcapitata (Korshikov) Hindák, and Chlorella fusca var. vacuolata Shihira et R. W. Kraus] using two neutral, nonionic probes, fluorescein diacetate (FDA) and D-sorbitol. In parallel experiments, we exposed algae to inorganic Cd or to Cd(DDC)2 (0) and monitored Cd intracellular metal distribution, together with phytochelatin synthesis. For the three algal species acclimated at pH 5.5 (w/wo DDC 1 μM) and exposed at this pH, their permeability to FDA and D-sorbitol was consistently lower than for algae growing at pH 7.0 and exposed at this pH (P < 0.001). The ratio of the FDA hydrolysis rate measured at pH 7.0 with respect to the rate measured at pH 5.5 (both in the presence of DDC) correlated with the ratio of the Cd(DDC)2 (0) initial internalization rate constant obtained at pH 7.0 versus that obtained at pH 5.5 (three algae species, n = 9, r = 0.85, P = 0.004). Our results strongly suggest that acidification affects metal availability to algae not only by proton inhibition of facilitated metal uptake but also by affecting membrane permeability.

The effect of pH on chronic aquatic nickel toxicity is dependent on the pH itself: Extending the chronic nickel bioavailability models

“…Alternatively, because Ni 2þ is most likely a Mg 2þ antagonist [34], Ni-carbonate complexes may potentially enhance uptake of Ni 2þ through a Mg 2þ /HCO 3 symporter, which has previously been characterized in tumor cells [35]. Additionally, a difference in pH can possibly alter the cell membrane integrity [36]. Finally, a nonlinear relation between H þ and Ni 2þ also may indicate the existence of more than 1 type of Ni 2þ binding site with different protonation constants, as was proposed for Cu toxicity to the amphipod Hyalella azteca [37].…”

When are metal complexes bioavailable?

“…Furthermore, uptake is sensitive to the pH of the medium, with a decreased bioaccumulation of the lipophilic metal complexes at low pH, potentially due to a reduction in the electrostatic repulsion between adjacent phospholipids, leading to their tighter packing and a decreased membrane permeability. [11,18,19] With the exception of what is known about such hydrophobic metal species as the methylated forms of Hg, Sn, As and Sb [20][21][22] and the hydrophobic complexes described above, it is currently unclear to what extent lipophilic ligands are present in natural systems. Owing in large part to the analytical difficulties associated with measurements of (likely low concentrations of) hydrophobic complexes in aquatic systems, few data are available to estimate metal uptake fluxes for these species.…”

“…Techniques such as solid-state nuclear magnetic resonance spectroscopy and synchrotron-based X-ray microscopy have been used to probe for the presence of ternary complexes on biological surfaces. For example, the formation of AlF x ternary complexes on cells obtained from fish gills (Micropterus salmoides) was demonstrated by 19 F nuclear magnetic resonance, [42] whereas Hg L III -edge X-ray absorption near-edge spectroscopy (XANES) showed that ternary complexes involving Hg-EDTA and the biological surface were unlikely. Experiments using radiolabelled ligands can also show when ligands are not taken up by the organism.…”

Importance de mieux connaître les mécanismes de transport des métaux pour la prédiction de l’accumulation et de la toxicité des métaux dissous chez le phytoplancton : récentes avancées et défis pour le développement du modèle du ligand biotique

“…En effet, quelques cas où le MLB ne pouvait prédire adéquatement la prise en charge et la toxicité des métaux chez les organismes aquatiques ont été retracés dans la littérature (CAMPBELL, 1995;CAMPBELL et al, 2002;SLAVEYKOVA et WILKINSON, 2005;ZHAO et al, 2016 (BOULLEMANT et al, 2009;FLORENCE et al, 1992;LAVOIE et al, 2012c;PHINNEY et BRULAND, 1994;STAUBER et FLORENCE, 1987 …”