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Marine microbes are major drivers of all elemental cycles. The processing of organic carbon by heterotrophic prokaryotes is tightly coupled to the availability of the trace element iron in large regions of the Southern Ocean. However, the functional diversity in iron and carbon metabolism within diverse communities remains a major unresolved issue. Using novel Southern Ocean meta-omics resources including 133 metagenome-assembled genomes (MAGs), we show a mosaic of taxonomy-specific ecological strategies in naturally iron-fertilized and high nutrient low chlorophyll (HNLC) waters. Taxonomic profiling revealed apparent community shifts across contrasting nutrient regimes. Community-level and genome-resolved metatranscriptomics evidenced a moderate association between taxonomic affiliations and iron and carbon-related functional roles. Diverse ecological strategies emerged when considering the central metabolic pathways of individual MAGs. Closely related lineages appear to adapt to distinct ecological niches, based on their distribution and gene regulation patterns. Our in-depth observations emphasize the complex interplay between the genetic repertoire of individual taxa and their environment and how this shapes prokaryotic responses to iron and organic carbon availability in the Southern Ocean.

Microbial iron and carbon metabolism as revealed by taxonomy-specific functional diversity in the Southern Ocean