The existence of a marine phosphorus (P) redox cycle was recently confirmed when phosphonates, organophosphorus compounds with P in the (III) oxidation state, were found in high molecular weight dissolved organic matter. Although some features of the P redox cycle have come to light since the discovery of phosphonates, many aspects of phosphonate production, cycling and fate remain unknown. To address these gaps in our understanding, we studied phosphonate cycling in the Eastern Mediterranean Sea, a chronically P-limited basin, using 33P and enzymatic assays. We showed that phosphonate production was low but consumption was high, suggesting that phosphonate production and consumption may be spatially or temporally decoupled. We also explored phosphonate production in the model marine cyanobacterium Prochlorococcus SB. Using 31P NMR, we found Prochlorococcus SB allocates ~50% of its cellular P to phosphonates. Allocation of P to phosphonates was conserved under P-limitation, and further investigation revealed phosphonates were associated with proteins. The discovery of phosphonoproteins in Prochlorococcus SB opens new perspectives on the biochemical function of phosphonates and their role in P-cycling. Finally, we developed a new P-targeted method to characterize marine organophosphorus compounds using liquid chromatography coupled to electrospray ionization and inductively coupled plasma mass spectrometry.