The Trace Metal Composition of Marine Phytoplankton

Twining, Benjamin S.; Baines, Stephen B.

doi:10.1146/annurev-marine-121211-172322

Cited by 443 publications

(529 citation statements)

References 134 publications

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“…Culturing experiments have demonstrated that the uptake of Cd into plankton-as with other divalent metalsoccurs in direct proportion to dissolved [Cd 2+ ], although this pattern can be modulated by competition with the availability of other metals (19,20). For example, Zn limitation has been shown to increase Cd uptake in bacteria (21) and phytoplankton (22)(23)(24), with Fe restriction also promoting an increase in cellular Cd quotas in culture (24,25).…”

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.

102

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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%

Nonspecific uptake and homeostasis drive the oceanic cadmium cycle

Horner

Lee

Henderson

et al. 2013

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

102

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“…However, recognizing these caveats, some interesting general patterns can still be discerned from consideration of a wider, albeit still limited subset of the nutrients ( figure 7). Phytoplankton have an absolute requirement for the micronutrient Mn, in part due to the presence of this element within the water splitting complex [2,27,45]. There is some direct [110,111] and indirect [112,113] evidence for the (co-)limiting potential of Mn within oceanic surface waters.…”

Section: (D) Deficiency Beyond N P and Fe: Mn And Znmentioning

confidence: 99%

Diagnosing oceanic nutrient deficiency

Moore¹

2016

Phil. Trans. R. Soc. A.

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“…Although the partial dissolution of the deposited particles increases the input of certain elements required for phytoplankton growth, an excess of these elements can be harmful to the extent that they negatively impact ecosystem health (7,8). For example, Cu is highly toxic even at relatively low concentrations (9), and its toxic effects can be exerted following its release from aerosol particles.…”

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confidence: 99%

Copper aerosols inhibit phytoplankton growth in the Mediterranean Sea

Jordi

Basterretxea

Tovar-Sánchez

et al. 2012

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

125

103

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Aerosol deposition plays an important role in climate and biogeochemical cycles by supplying nutrients to the open ocean, in turn stimulating ocean productivity and carbon sequestration. Aerosol particles also contain elements such as copper (Cu) that are essential in trace amounts for phytoplankton physiology but that can be toxic at high concentrations. Although the toxicity of Cu associated with aerosols has been demonstrated in bioassay experiments, extrapolation of these laboratory results to natural conditions is not straightforward. This study provides observational evidence of the negative effect of aerosols containing high Cu concentrations on marine phytoplankton over a vast region of the western Mediterranean Sea. Direct aerosol measurements were combined with satellite observations, resulting in the detection of significant declines in phytoplankton biomass after atmospheric aerosol events characterized by high Cu concentrations. The declines were more evident during summer, when nanoflagellates predominate in the phytoplankton population and stratification and oligotrophic conditions prevail in the study region. Together with previous findings concerning atmospheric Cu deposition, these results demonstrate that the toxicity of Cu-rich aerosols can involve large areas of the world's oceans. Moreover, they highlight the present vulnerability of oceanic ecosystems to Cu-rich aerosols of anthropogenic origins. Because anthropogenic emissions are increasing, large-scale negative effects on marine ecosystems can be anticipated.atmospheric dust | trace metal

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The Trace Metal Composition of Marine Phytoplankton

Cited by 443 publications

References 134 publications

Nonspecific uptake and homeostasis drive the oceanic cadmium cycle

Nonspecific uptake and homeostasis drive the oceanic cadmium cycle

Diagnosing oceanic nutrient deficiency

Copper aerosols inhibit phytoplankton growth in the Mediterranean Sea

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