ABSTRACTThe marine unicellular cyanobacteriumProchlorococcusis 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 thatProchlorococcushigh-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 purines in RNA and DNA. Genes encoding the predicted phosphonate oxidative pathway of MIT9301 were predominantly present inProchlorococcusgenomes from parts of the North Atlantic Ocean where phosphate availability is typically low, suggesting that phosphonate oxidation is an ecosystem-specific adaptation of someProchlorococcuspopulations to cope with phosphate scarcity.IMPORTANCEUntil recently, 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 planctomyceteGimesia maris(S. R. Gama, M. Vogt, T. Kalina, K. Hupp, et al., ACS Chem Biol 14:735–741, 2019,https://doi.org/10.1021/acschembio.9b00024) and the presence of this pathway inProchlorococcusindicate 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 byProchlorococcusmay direct the flow of this one-carbon compound to carbon dioxide or assimilation into biomass, thus limiting the production of methane.
Small Phytoplankton Shapes Colored Dissolved Organic Matter Dynamics in the North Atlantic Subtropical Gyre