Extensive and diverse lanthanide-dependent metabolism in the ocean

Abstract

To date, the only known Lanthanide (Ln)-dependent enzymes are pyrroloquinoline quinone-dependent alcohol dehydrogenases. When compared to their Ca dependent counterparts, there is an emerging picture that Ln-dependent versions of these enzymes are generally more efficient, are preferentially upregulated in the presence of Ln when there is functional redundancy, and may even be evolutionarily older. Ln-utilising microbes have furthermore evolved diverse means of solubilizing and acquiring Ln, enabling them to utilise Ln even at trace concentrations. The ocean is the largest dissolved organic carbon pool on Earth, yet the diversity and prevalence of Ln-dependent carbon metabolisms in the ocean is unknown. Here we show that Ln-utilising methanol-, ethanol- and putative sorbose- and glucose-dehydrogenase genes are ubiquitous in the ocean and are highly transcribed, despite extremely low concentrations of Ln in seawater. These enzymes occur in the genomes of 20% of marine microbes, with several individual organisms hosting dozens of unique Ln-utilising enzymes. We found that active microbial methanol oxidation in the ocean is almost entirely Ln-dependent. The widespread biological utility of Ln may help to explain the nutrient-like vertical concentration profiles of these elements in ocean waters and may exert an influence on rare earth element concentration patterns. Microbial Ln-utilisation is a poorly understood component of marine rare earth element biogeochemistry, with potentially important implications for the carbon cycle. The ocean microbiome will be a rich resource for future research into biologically inspired solutions to lanthanide extraction and purification.