Methylphosphonate oxidation in Prochlorococcus supports phosphate acquisition, formate excretion, and carbon assimilation into purines

The marine unicellular cyanobacterium Prochlorococcus is an abundant primary producer and widespread inhabitant of the photic layer in tropical and subtropical marine ecosystems where the inorganic nutrients required for growth are limiting. In this study we demonstrate that Prochlorococcus high-light strain MIT9301, an isolate from the phosphate-depleted subtropical North Atlantic Ocean, can oxidize methylphosphonate (MPn) and hydroxymethylphosphonate (HMPn), two phosphonate compounds present in marine dissolved organic matter, to obtain phosphorus. The oxidation of these phosphonates releases the methyl group as formate which is both excreted and assimilated into purine nucleotides in RNA and DNA. Genes encoding the predicted phosphonate oxidative pathway of MIT9301 were predominantly present in Prochlorococcus genomes from the North Atlantic Ocean where phosphate availability is typically low suggesting that phosphonate oxidation is an ecosystem-specific adaptation of some Prochlorococcus populations to cope with phosphate scarcity. Importance Until recently, methylphosphonate (MPn) was only known to be degraded in the environment by the bacterial carbon-phosphorus (CP) lyase pathway, a reaction that releases the greenhouse gas methane. The identification of a formate-yielding MPn oxidative pathway in the marine planctomycete Gimesia maris (Gama et al , ACS Chem Biol, 2019, doi: 10.1021/acschembio.9b00024) and the presence of this pathway in Prochlorococcus indicates that this compound can follow an alternative fate in the environment while providing a valuable source of P to organisms. In the ocean, where MPn is a major component of dissolved organic matter, the oxidation of MPn to formate by Prochlorococcus may direct the flow of this one-carbon compound to carbon dioxide or assimilation into biomass, thus limiting production of methane.