Microbial utilization of rare earth elements at cold seeps related to aerobic methane oxidation

Abstract

A major breakthrough in the field of rare earth element (REE) geochemistry has been the recent discovery of their utility to microbial life, as essential metalloenzymes catalyzing the oxidation of methanol to formaldehyde. Lanthanide-dependent bacteria are thought to be ubiquitous in marine and terrestrial environments, but direct field evidence of preferential microbial utilization of REE in natural systems is still lacking. In this study, we report on the REE and trace element composition of the tube of a siboglinid worm collected at a methane seep in the Gulf of Guinea; a tube-dwelling annelid that thrives in deep-sea chemosynthetic ecosystems. High-resolution trace element profiles along the chitin tube indicate marked enrichments of lanthanum (La) and cerium (Ce) in its oxic part, resulting in REE distribution patterns that depart significantly from the ambient seawater signature. Combined with various geochemical and microbiological evidence, this observation provides direct support for an active consumption of light-REE at cold seeps, associated with the aerobic microbial oxidation of methane. To further evaluate this hypothesis, we also re-examine the available set of REE data for modern seep carbonates worldwide. While most carbonate concretions at cold seeps generally display REE distribution patterns very similar to those for reduced pore waters in marine sediments, we find that seafloor carbonate pavements composed of aragonite commonly exhibit pronounced light-REE enrichments, as inferred from high shale-normalized La/Gd ratio (>~0.8), interpreted here as possibly reflecting the signature of lanthanide-dependent methanotrophic activity. This finding opens new perspectives for revisiting REE systematics in ancient seep carbonates and other microbialites throughout the Earth's history. In particular, the geochemical imprint of aerobic methane oxidation could be possibly traced using REE in Archaean stromatolites and other archives of Precambrian seawater chemistry, potentially providing new insights into the oxygenation of early Earth's oceans and associated microbiogeochemical processes.