Phytochelatin production in marine algae. 2. Induction by various metals

Ahner, Beth A.; Morel, Françios M. M.

doi:10.4319/lo.1995.40.4.0658

Cited by 193 publications

(130 citation statements)

References 19 publications

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“…E. coli, which lack a vacuole, translocate Cd to their membranes (35) by binding Cd with glutathione, a precursor of (and functionally analogous to) phytochelatin (28). Cd is a particularly efficient metal for inducing production of metal-binding ligands in plankton (36), with analysis of field populations (37,38) and laboratory cultures (39,40) demonstrating that Cdbinding ligands are produced far in excess of that needed to sequester any intracellular Cd (and other metals, such as Cu and Zn; ref. 36).…”

Section: Discussionmentioning

confidence: 99%

“…Cd is a particularly efficient metal for inducing production of metal-binding ligands in plankton (36), with analysis of field populations (37,38) and laboratory cultures (39,40) demonstrating that Cdbinding ligands are produced far in excess of that needed to sequester any intracellular Cd (and other metals, such as Cu and Zn; ref. 36). Our isotope data demonstrate that this process of homeostasis can lead to the retention of isotopically light inert Cd complexes by organisms (Fig.…”

Section: Discussionmentioning

confidence: 99%

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Nonspecific uptake and homeostasis drive the oceanic cadmium cycle

Horner

Lee

Henderson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

103

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The global marine distributions of Cd and phosphate are closely correlated, which has led to Cd being considered as a marine micronutrient, despite its toxicity to life. The explanation for this nutrient-like behavior is unknown because there is only one identified biochemical function for Cd, an unusual Cd/Zn carbonic anhydrase. Recent developments in Cd isotope mass spectrometry have revealed that Cd uptake by phytoplankton causes isotopic fractionation in the open ocean and in culture. Here we investigate the physiochemical pathways that fractionate Cd isotopes by performing subcellular Cd isotope analysis on genetically modified microorganisms. We find that expression of the Cd/Zn carbonic anhydrase makes no difference to the Cd isotope composition of whole cells. Instead, a large proportion of the Cd is partitioned into cell membranes with a similar direction and magnitude of Cd isotopic fractionation to that seen in surface seawater. This observation is well explained if Cd is mistakenly imported with other divalent metals and subsequently managed by binding within the cell to avoid toxicity. This process may apply to other divalent metals, whereby nonspecific uptake and subsequent homeostasis may contribute to elemental and isotopic distributions in seawater, even for elements commonly considered as micronutrients.biological fractionation | isotope geochemistry | metal homeostasis | subcellular analysis | trace metal I n addition to the macronutrients nitrate, phosphate, and silicate, marine phytoplankton require many essential metals to function correctly (1). The uptake and utilization of these micronutrients results in large vertical isotopic and concentration gradients for many transition metals in seawater (2). In the open ocean, Cd concentrations are as low as a few picomoles per kilogram (2, 3), with associated highly fractionated Cd isotopic compositions of up to several permil ( Fig. 1) (4). In culture, phytoplankton consume small quantities of Cd (5-7) and exhibit light Cd isotope compositions (8). Taken together, the available data suggest that the marine geochemistry of Cd is dominated by nutrient-like processes (i.e., required uptake). However, only one biochemical function for Cd is known: CdCA1, a Cd/Zn carbonic anhydrase from the marine diatom Thalassiosira weissflogii (9, 10). Although ubiquitous in natural waters (11), CdCA1 is absent in numerous phytoplankton including coccolithophores, cyanobacteria, archaea, and several species of diatom (11) (Table S1), and it is thus debateable whether the expression of this single enzyme can account for the nutrient-like distribution of Cd in the global ocean. Here we examine the isotopic fractionation of Cd associated with CdCA1 that has been expressed in vivo by the model microorganism, Escherichia coli. Because E. coli has no inherent use for Cd, our experimental design permits comparison of cultures both overexpressing and not expressing CdCA1 in otherwise identical experiments. Using a systematic experimental approach, we are able to identify ...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Nonspecific uptake and homeostasis drive the oceanic cadmium cycle

Horner

Lee

Henderson

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

103

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“…Other compounds thought to be released by algae in cultures include phytochelatins (Ahner and Morel 1995;Scarano and Morelli 1996) and lumichrome (a photolysis product of riboflavin) (Morelli and Scarano 1994). Lumichrome has a peak potential of Ϫ0.68 V, similar to that of thioacetamide.…”

Section: Release Of Complexing Ligands By the Algae-duringmentioning

confidence: 99%

Copper‐induced release of complexing ligands similar to thiols by Emiliania huxleyi inseawater cultures

Leal

Vasconcelos

Berg

1999

Limnology & Oceanography

179

121

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Marine microalgae (Emiliania huxleyi) were grown in seawater enriched only with nitrogen and phosphorus, without control of free metal concentrations using synthetic chelators. Complexing ligands and thiol compounds were determined by cathodic stripping volt-ammetry. Copper was added to these cultures, and ligands were produced in response to the copper addition. Parallel measurements of thiols showed that glutathione and other unidentified thiols (electrochemically similar to thioacetamide) were produced by the algae at rates and concentrations similar to those of the complexing ligands. Smaller amounts of thiols were produced when ligands including thiols were added to the culture. The results indicate that thiols can account for a major part or most of the copper-complexing ligands produced by these algae. Furthermore, a feedback mechanism exists in which the production of thiol-type complexing ligands is controlled by the free copper concentration, production already being stimulated by an increase of [Cu 2ϩ ] from 0.4 to 1.5 pM. Incubations with added exudates, thiols, and salicylaldoxime (SA) showed much reduced copper toxicity even though copper uptake was increased by the exudates and the SA.Culture experiments have shown that marine and freshwater phytoplankton release complexing ligands into culture medium (e.g., van den Berg et al. 1979;Imber and Robinson 1983), which may be important because the availability of metals to algae is known to depend on their chemical composition (e.g., Brand et al. 1983). Therefore, the interaction of phytoplankton with trace metals is reciprocal: the biota affect the trace metal chemistry and the trace metals affect the biota.Using marine algal cultures where the metal chemistry was controlled by a synthetic chelator (usually ethylenediaminetetraacetic acid [EDTA]), the biological uptake of copper has been shown to be related to the cupric ion concentration, [Cu 2ϩ ] (e.g., Brand et al. 1986); toxicity occurs at pM levels of Cu 2ϩ . The concentration of Cu 2ϩ is typically lowered by by 2-3 orders of magnitude by organic complexation in seawater to a [Cu 2ϩ ] of 0.03-0.3 pM, which is thought to be sufficiently high to meet algal nutritional requirements but is below copper toxicity levels (Sunda 1995).

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“…phytochelatins, metallothioneins) or metal deficiency (e.g. siderophores), and can be released into the water either in response to metal exposure or following cell lysis [125][126][127]. Nonetheless, most of the information on biologically produced, chelating molecules has come from laboratory culture studies, e.g.…”

Section: Nature Of Metal Complexes In Aquatic Systemsmentioning

confidence: 99%