Phosphate-related genomic islands as drivers of environmental adaptation in the streamlined marine alphaproteobacterial HIMB59

Prokaryotic species are composed of multiple clonal lineages coexisting in the same habitat. In recent years, understanding the maintenance of this high intraspecific genetic diversity in asexual microorganisms has been a challenge for microbial ecology. In this study, we investigated the potential ecological role of this genomic heterogeneity in the marine HIMB59 clade. The metagenomic recruitment revealed the presence of three main genomospecies with different ecological distribution patterns within the two defined families. Genomic analysis revealed the presence of a flexible genomic island conserved throughout the order at the same position in the genome and related to phosphate (P) metabolism. The different versions of this island showed a distribution correlated with the concentration of P in the environment but not with the phylogeny at the genomospecies level. At high P availability (>0.5 mu M), HIMB59 cells had only the high-affinity phosphate transporter operon (PstSCAB and PhoU). Under conditions of higher P scarcity (<0.05 mu M), the cells presented a higher number of genes for the acquisition of P groups from other sources such as organic molecules and their storage. Additionally, in oligotrophic regions exhibiting extreme P depletion, such as the Mediterranean Sea, we found a second flexible genomic island related to phosphonate catabolism to supply metabolic P requirements. These results suggest that these microbes maintain in natural populations a gene pool with an equivalent biological function that allows them to respond to variations in certain micronutrients, creating ecologically distinct lineages within each species.