This is a 'preproof' accepted article for Mineralogical Magazine. This version may be subject to change during the production process.
Prior to soil formation, phosphate liberated by rock weathering is often sequestered into highly insoluble lanthanide phosphate minerals. Dissolution of these minerals is critical for the release of phosphate to the biosphere, yet the microorganisms involved, and the genes required for lanthanide metabolism, are poorly understood. Here, we sampled weathered granite and associated soil to identify the zones of lanthanide phosphate mineral solubilization and genomically define the organisms implicated in lanthanide utilisation. We reconstructed 136 genomes from 11 bacterial phyla and found gene clusters implicated in lanthanide-based metabolism of methanol (primarily XoxF3 and XoxF5) are surprisingly common in microbial communities in moderately weathered granite where lanthanide phosphate minerals are dissolving. Notably, XoxF3 systems were found in Verrucomicrobia for the first time, and in Acidobacteria, Gemmatimonadetes, and Alphaproteobacteria. The XoxF-containing gene clusters are shared by diverse Acidobacteria and Gemmatimonadetes, and include conserved hypothetical proteins and transporters not associated with the few well studied XoxF systems. Given that siderophore-like molecules that strongly bind lanthanides may be required to solubilize lanthanide phosphates, it is notable that candidate siderophore biosynthesis systems were most prevalent in bacteria in moderately weathered rock, especially in Acidobacteria with lanthanide-based systems. We conclude that the confluence in the zone of moderate weathering of phosphate mineral dissolution, lanthanide utilisation, and methanol oxidation (thus carbonic acid production) may be important during the conversion of granitic rock to soil.
Lanthanide (Ln)-dependent enzymes have evolved roles in organic carbon metabolism despite low Ln availability in natural environments. 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 Earth's 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.
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