Metal binding properties of the EPS produced by Halomonas sp. TG39 and its potential in enhancing trace element bioavailability to eukaryotic phytoplankton

Abstract

An emergent property of exopolysaccharides (EPS) produced by marine bacteria is their net negative charge, predominantly conferred by their high uronic acids content. Here, we investigated the EPS produced by an algal-associated marine bacterium, Halomonas sp. strain TG39, for its capacity to sequester trace metals and mediate their bioavailability to eukaryotic phytoplankton. Metal analysis of the purified EPS revealed that it contained high levels of K, Ca, Mg and several essential trace metals, including Zn, Cu, Fe and the metalloid Si. Desorption experiments with marine sediment showed that the EPS possessed a specific binding capacity for Ca, Si, Fe, Mn, Mg and Al. Depending on the ionic conditions, Fe was the third or fourth most highly-adsorbed metal out of 27 elements analyzed. Experiments employing Fe-limited synthetic ocean seawater showed that growth of the marine diatom Thalassiosira weissflogii (axenic strain) was enhanced when incubated in the presence of either purified EPS or EPS that had been pre-exposed to marine sediment, compared to non-EPS amended controls. This growth enhancement was attributed to the EPS binding and increasing the bioavailability of key trace metal elements, such as Fe(III). Since the bacterium used in this study was originally isolated from a marine micro-alga, this work highlights the possibility that bacterial associates of eukaryotic algae could be influencing the bioavailability of Fe(III) to phytoplankton via their production of polyanionic EPS. More widely, this work reinforces the potential importance of marine bacterial EPS in trace metal biogeochemical cycling.