The effect of pH on the uptake of zinc and cadmium in marine phytoplankton: Possible role of weak complexes

Abstract

In natural samples from the New Jersey coast and the Gulf of Alaska, zinc (Zn) and cadmium (Cd) uptake rates by phytoplankton decreased on average about 30% as pH was decreased from 8.5 to 7.9 or 7.7, and the partial pressure of carbon dioxide (PCO2) increased accordingly. The underlying mechanism was explored with the model species, Thalassiosira weissflogii and Emiliania huxleyi, using ethylenediaminetetraacetic acid (EDTA), desferrioxamine B, phytochelatin, and cysteine as complexing agents. Experiments with single complexing agents did not reproduce the effect of pH seen in field samples, ruling out two possible mechanisms: a direct effect on the uptake machinery or down‐regulation of uptake at high PCO2. Zn and Cd bioavailability must thus somehow decrease at low pH in natural seawater, which is counterintuitive since the protonation of complexing agents at low pH should increase the total free concentration of metals. However, in the presence of both a strong and a weak complexing agent, metal uptake rate may decrease at low pH if formation of the weak complex decreases and the metal in the weak complex is more “available” than in the strong complex. We obtained proof of concept for such a two‐ligand mechanism for Zn uptake in the presence of EDTA + phytochelatin and EDTA + cysteine. Weak ligands that bind a small fraction of essential metals in surface seawater may thus be important in metal uptake by phytoplankton, and the dual effects of strong and weak complexing agents may control not just the magnitude but also the sign of the effect of pH‐PCO2 on metal uptake rates.

Ocean acidification slows nitrogen fixation and growth in the dominant diazotroph Trichodesmium under low-iron conditions

“…In view of the large effect of pH variations on metal uptake demonstrated here and in other studies (4,42), it is possible that the positive effect of high pCO 2 commonly observed on Trichodesmium cultured in YBCII may be caused by changes in the bioavailability of essential or toxic metals. This positive effect also likely reflects the energy savings afforded by a down-regulation of the CCM, as usually has been inferred (43).…”

Effects of indirect toxicity of interacting Cd–Zn in a planktonic marine system

“…Therefore, if food density available in the environment can modify the observed total toxic effect at the population level, eutrophic environments may be especially vulnerable to the discharge of inorganic substances such as metals, with interactive negative effects on consumer populations. This is particularly because the Zn and Cd requirements of the organisms or the uptake of the metals may be indirectly affected by detrimental environmental conditions caused by an increase of organic matter (Xu et al 2012).…”

“…Under an individualistic approach it has been shown that most of the Zn found in copepods is obtained from ingested food, with higher assimilation efficiency at low food concentrations, while most of the Cd accumulates from the dissolved phase (Wang et al 1996, Wang & Fisher 1998. Nevertheless, the relative importance of trace element uptakes from the dissolved phase versus food ingestion in overall metal uptake depends on many specific consumer−resource traits and environmental conditions, making it difficult to determine general patterns and to predict effects (Langston & Spence 1995, Xu et al 2012.…”

“…Earlier evidence suggested that the combined effect of Cd and Zn at high concentrations could be lethal at any trophic level (Elinder & Piscator 1978, Wolter et al 1984, Lee & Morel 1995, Aravind & Vara 2005, Juárez-Franco et al 2007). As Cd is known to replace Zn for some biological functions in a selection of phytoplankton species (Lane & Morel 2000, Xu et al 2012), a certain degree of interaction between these metals is expected.…”

“…Cd is a highly toxic heavy metal (Tortell & Price 1996, Nassiri et al 1997, the effects of which may be observed at several trophic levels of marine food webs, including microand macroalgae, zooplankton, molluscs and crustaceans (Elinder & Piscator 1978, Nassiri et al 1997, Juárez-Franco et al 2007). On the other hand, although Zn is an essential micronutrient for phytoplankton, which is used as a cofactor in many enzymes (Aravind & Vara 2005, Xu et al 2012, at high concentrations it may be toxic (Juárez-Franco et al 2007). Earlier evidence suggested that the combined effect of Cd and Zn at high concentrations could be lethal at any trophic level (Elinder & Piscator 1978, Wolter et al 1984, Lee & Morel 1995, Aravind & Vara 2005, Juárez-Franco et al 2007).…”