On the biological meaning of the population pangenome

The prokaryotic pangenome, the full complement of genes within a species, is strikingly large. To understand how ecological forces shape this diversity, it is useful to examine the variable gene pool within a single population, defined as cells of the same species coexisting in the same time and place. This single-population pangenome reflects the minimal flexible gene repertoire required in a specific environmental context. Recent long-read metagenomic studies of marine prokaryotes show that local population pangenomes remain large, often comprising thousands of genes. Specifically, cells belonging to the same species of the streamlined alfaproteobacterium Pelagibacter, coming from the same sampling site and even sample, contain more than a thousand genes. Many of these genes are related variants that collectively expand the population's metabolic potential, akin to paralogs within a single large genome. We propose for them the name 'metaparalogs' together with the idea that these data reflect cooperative, population-level strategies, where the flexible genome operates as a public good (sensu Samuelson), enhancing both adaptability and ecological resilience. A role for extracellular vesicles in facilitating resource sharing is also suggested.