Homeostasis drives intense microbial trace metal processing on marine particles

As marine microorganisms and environmental conditions coevolved over geological timescales, metals have been incorporated into all essential metabolic processes. In the modern ocean, metals are present from trace amounts limiting microbial growth to toxic concentrations. Dissolved trace metals are a major bioavailable reservoir. However, the acquisition of metals from marine particles remains largely unexplored. Here, we combined chemical characterization and a comparative metatranscriptomics approach to investigate the availability of nine metals of biological importance on particles collected in the region of Heard Island (Indian sector of the Southern Ocean). Elemental ratios identified particulate matter as a potential source of metals for prokaryotes. The expression of genes for the uptake of metals through various mechanisms demonstrated that particles are a bioavailable reservoir. But genes involved in the control of resistance to metal toxicity, storage, sensing, and regulation were also highly expressed. Our observations suggest that homeostasis associated with a diverse prokaryotic community is the overarching mechanism that enhances the trace element processing on particles. These results provide clues that microbial activity on particles is critical in the redistribution of trace elements between different fractions and chemical forms in the ocean.