Large diversity in the O-chain biosynthetic cluster within populations of Pelagibacterales

Abstract

Genomic diversity in prokaryotic species is largely due to the existence of extensive pangenomes, allowing different gene complements to be drawn depending on the strain. Here, we have studied the diversity of the O-chain polysaccharide biosynthesis cluster (OBC) in marine bacteria of the Pelagibacterales order as a proxy to measure such genetic diversity in a single population. The study of single-amplified genomes (SAGs) from the whole order found a pattern similar to that of other well-studied microbes, such as the Enterobacteriales or Alteromonas, where distinct OBCs represent strains containing different gene pools. We found that most of the OBC sharing happened among individuals of the same clonal frame (>99% average nucleotide identity). Moreover, given the parsimonious way this cluster changes, the diversity of the OBCs can be extrapolated to the size of the population’s pangenome. This assumes that different OBCs correspond to lineages containing unique flexible gene pools, as seen in the aforementioned microbes. Through long-read metagenomics, we could detect 380 different OBCs at a single Mediterranean sampling site. Within a single population (single species and sample) of the endemic Ia.3/VII (gMED) genomospecies, we identified 158 OBCs, of which 130 were unique. These findings suggest that the gene pool within a single population might be substantial (several thousands). While this figure is large, it aligns with the complexity of the dissolved organic matter that these organisms can potentially degrade.