Global geography outweighs long-term dynamics in shaping marine microbial population structure

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Abstract
Marine microbial populations play essential roles in ocean ecosystems, yet the processes shaping their genomic structure across space and time remain poorly understood. Here, we examined the population-scale patterns of 1,505 prokaryotic metagenome-assembled genomes (MAGs) retrieved from the Northwestern Mediterranean Sea in two long-term coastal time series, along 15 and 7 years in these sites, as well as in the global ocean. We found that populations were generally more genomically differentiated across large spatial scales than across long temporal scales. Among a subset of 389 MAGs well represented in all datasets, 68.4% showed weak population divergence over time but strong global-scale differentiation. This was evident in the abundant and widespread cyanobacteria Prochlorococcus and Synechococcus. In contrast, only 6.4% of the MAGs exhibited weak divergence over time and space, with SAR11 MAGs being a clear example, likely reflecting their high dispersal and recombination rates. Other groups, such as SAR86 and Flavobacteriales, showed strong divergence at temporal and spatial scales, suggesting seasonal and/or regional adaptation. Positive selection was more readily detectable in the long-term coastal observatories than in the global ocean, despite the more significant population divergence observed across broad geographic scales. Temperature consistently showed a significant association with the population structure of many MAGs. Overall, our results highlight the dominant influence of large geographic scales in shaping microbial population structure alongside taxon-specific responses to temporal variation, particularly seasonality. Altogether, our work advances the understanding of microbial population structure across broad spatial and temporal scales, a critical step toward predicting microbial dynamics in a changing ocean.
Funding Information
  • Ministerio de Economía, Comercio y Empresa, Madrid, ES (RYC-2013-12554)
  • Ministerio de Economía, Comercio y Empresa, Madrid, ES (CTM2015-69936-P)