Nonspecific uptake and homeostasis drive the oceanic cadmium cycle

Abstract

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 ...

Reply to Morel: Cadmium as a micronutrient and macrotoxin in the oceans

“…Our data demonstrate that microbial metal homeostasis-in vivo binding of Cd by GSH-causes Cd-isotope fractionation and leads to the retention of inert isotopically light Cd complexes by microorganisms. The magnitude of Cdisotope fractionation observed during microbial metal homeostasis is consistent with patterns of Cd-isotope fractionation seen in the modern ocean (2).…”

“…This is based on the observation that, in our experiments, the Cd-isotopic composition of cultured microbes was independent of the presence/absence of the CdCA1 metalloenzyme (Cd carbonic anhydrase; the only known biochemical function for Cd). Whole-cell Cd-isotope compositions were quantitatively driven by the intracellular sequestration of isotopically light Cd to cell membranes (2). We interpret this sequestration as evidence of microbial Cd homeostasis, which is a ubiquitous and highly conserved process across all forms of life.…”

Diagnosing oceanic nutrient deficiency

“…variable values for R X:Y ) which can be observed in cultures of marine phytoplankton [12,45], as well as within marine organic matter and the biogeochemical imprints of some BCP-related processes [45][46][47][48], further complicates the interpretation of combined tracers (X Y *). Stoichiometric plasticity is particularly acute for the trace metals due to non-specific uptake [12,[49][50][51][52] and the so-called 'luxury' uptake [53,54], alongside multiple mechanisms for reducing quotas under conditions where a nutrient becomes limiting, including the use of metabolically substitutable alternative nutrient elements [18,55]. Consequently, use of Fe P *, for example, has largely been limited to that of a diagnostic tracer within models where the biological stoichiometry is fixed at an assumed value [38].…”

Goldilocks and the three inorganic equilibria: how Earth’s chemistry and life coevolve to be nearly in tune

“…Despite the inference that the earliest enzymes were likely cambialistic and evolved towards specificity [25], the relative scarcity of CDCA, so far found only with the diatom class of algae [26], speaks to the geologically recent novelty in the use of trace metals for life. Whether the uptake of Cd into CDCA accounts quantitatively for the global correlation between Cd and phosphate remains contentious [27,28]. A question for future research will be to disentangle from the widely explored biological quota of metals for phytoplankton [29], and inference of nutrient-like metals from seawater profiles, the entwined absolute requirement of metals for life from the biological sequestration of mistakenly imported metals.…”