Background <p>Trace metals are co-factors for enzymes that are essential for microbial metabolism and the cycling of major elements. Membrane transporters allow microbes to sense and react to trace elements in the environment and to balance their uptake and export for the regulation of intracellular metal homeostasis. The acquisition and efflux of trace metals could lead to reciprocal feedbacks between microbes and the surrounding environment. Whether these processes vary among trace metals and across habitats is presently not known. We used membrane transporters into and out of the cell as indicators for the uptake and efflux of trace metals and provide a detailed picture of the distribution of the respective genes in distinct provinces in surface waters and in subsurface water masses across a transect in the Southern Indian Ocean.</p> Results <p>We observed marked spatial and vertical patterns in normalized gene abundances of transporters of iron (Fe), manganese (Mn), nickel (Ni) and copper (Cu). Changes in gene abundances were specific to the type of transporter and trace metal, and pronounced differences between surface and specific water masses emerged. We found an enrichment in genes related to efflux and homeostasis of Fe, Ni and Cu in two water masses of the deep ocean that are North Atlantic Deep Water (NADW) and Lower Circumpolar Deep Water (LCDW). This pattern was observed on the community level and for metagenome-assembled&#xa0;genomes (MAGs) affiliated with <i>Alteromonadaceae</i> and <i>Burkholderiaceae</i> that were abundant in these two water masses.</p> Conclusions <p>The enrichment in trace metal efflux and resistance genes points to microbially mediated processes, exerted by homeostasis, with potential influence on the trace metal speciation and distribution in specific water masses in the deep ocean. The gene repertoire and distinct distribution pattern of the taxa identified as potential key players could reflect an adaptation to these old water masses with trace metals acting as selective driver.</p> <p><MediaObject ID="MOESM11"> <VideoObject FileRef="MediaObjects/40168_2025_2293_MOESM11_ESM.mp4" VideoID="6eGbYp9i1LptG_pNuhjymd"> <Caption Language="En" xml:lang="en"> <CaptionContent> <p>Video Abstract</p> </CaptionContent> </Caption> </VideoObject> </MediaObject></p>

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Microbial membrane transporters reveal trace metal niche adaptation in distinct water masses of the Southern Ocean

  • Rui Zhang,
  • Pavla Debeljak,
  • Sharvari Sunil Gadegaonkar,
  • Corentin Baudet,
  • Antoine Ringard,
  • Stéphane Blain,
  • Ingrid Obernosterer

摘要

Background

Trace metals are co-factors for enzymes that are essential for microbial metabolism and the cycling of major elements. Membrane transporters allow microbes to sense and react to trace elements in the environment and to balance their uptake and export for the regulation of intracellular metal homeostasis. The acquisition and efflux of trace metals could lead to reciprocal feedbacks between microbes and the surrounding environment. Whether these processes vary among trace metals and across habitats is presently not known. We used membrane transporters into and out of the cell as indicators for the uptake and efflux of trace metals and provide a detailed picture of the distribution of the respective genes in distinct provinces in surface waters and in subsurface water masses across a transect in the Southern Indian Ocean.

Results

We observed marked spatial and vertical patterns in normalized gene abundances of transporters of iron (Fe), manganese (Mn), nickel (Ni) and copper (Cu). Changes in gene abundances were specific to the type of transporter and trace metal, and pronounced differences between surface and specific water masses emerged. We found an enrichment in genes related to efflux and homeostasis of Fe, Ni and Cu in two water masses of the deep ocean that are North Atlantic Deep Water (NADW) and Lower Circumpolar Deep Water (LCDW). This pattern was observed on the community level and for metagenome-assembled genomes (MAGs) affiliated with Alteromonadaceae and Burkholderiaceae that were abundant in these two water masses.

Conclusions

The enrichment in trace metal efflux and resistance genes points to microbially mediated processes, exerted by homeostasis, with potential influence on the trace metal speciation and distribution in specific water masses in the deep ocean. The gene repertoire and distinct distribution pattern of the taxa identified as potential key players could reflect an adaptation to these old water masses with trace metals acting as selective driver.

Video Abstract