Extensive and diverse lanthanide-dependent metabolism in the ocean

Abstract

Lanthanide (Ln)-dependent enzymes have evolved roles in organic carbon metabolism despite low Ln availability in natural environments1-8. The oceans are the major reservoir of dissolved organic carbon (DOC) on the planet, yet the prevalence and diversity of Ln-dependent enzymes in the ocean, and their biogeochemical importance in the ocean carbon cycle is unknown. Here, we analyzed a global ocean metagenomic/metatranscriptomic dataset and found Ln-dependent methanol-, ethanol- and putative sorbose- and glucose-dehydrogenases in all metagenomes and 20% of all resolved microbial genomes, with several individual organisms hosting dozens of unique Ln-dependent genes. We find that biological methanol oxidation in the ocean is overwhelmingly Ln-dependent, and that methanol dehydrogenases are the most highly expressed Ln-dependent genes in most ocean regions, particularly in surface oceans. As Ln availability is a function of phosphate concentration and pH, Ln-dependent metabolism likely underpins complex biogeochemical feedbacks determining the efficiency of organic matter remineralization, thus impacting the oceanic DOC pool and Earths climate system. The widespread biological utility of Ln also explains their nutrient-like vertical concentration profiles observed in ocean waters, and shows that the preferential utilization of light lanthanides by biology must be considered when interpreting patterns of relative Ln concentrations in seawater.