Phosphonate degradation through the C-P lyase pathway by a dinoflagellate-associated Mameliella alba enhances host growth under phosphate limitation.

Phosphonates are distinguished by their chemically stable carbon-phosphorus (C-P) bonds and constitute approximately 25% of the dissolved organic P pool in the ocean. Most eukaryotic phytoplankton, including dinoflagellates, are unable to directly utilize extracellular phosphonates. However, their associated bacteria can facilitate indirect exploitation of this P source. This study presents the isolation and characterization of strain DH-1, a dinoflagellate-associated bacterium capable of phosphonate degradation. DH-1 was identified as Mameliella alba, and its genome contains a complete C-P lyase gene cluster. Growth assays demonstrated that DH-1 could maintain growth under conditions with 2-aminoethylphosphonate (2-AEP) as the sole P source, indicating that it can utilize this biogenic phosphonate. RT-qPCR analyses revealed that transcription levels of the C-P lyase subunits phnJ and phnH, as well as the phosphonate transport genes phnC and phnD, were significantly upregulated under phosphate-limited conditions. Furthermore, the expression of phnJ and phnH was also induced by 2-AEP, indicating that C-P lyase pathway in DH-1 is co-regulated by the Pho regulon and substrate induction. The growth of the dinoflagellate Prorocentrum donghaiense was significantly enhanced when both DH-1 and 2-AEP were added to P-limited cultures, whereas the alga did not grow in the presence of either 2-AEP or DH-1 alone. This study presents the first example of a specific dinoflagellate-associated bacterium that can promote algal growth by degrading phosphonates to release phosphate. These interactions are vital for the ecological success of dinoflagellates that live in P-limited environments, offering novel insights into the formation and dynamics of harmful algal blooms.IMPORTANCEPhosphonates are an important component of dissolved organic phosphorus in the ocean. They can serve as a potential phosphorus source when phosphate, which is directly bioavailable to phytoplankton, is scarce in marine environments. While eukaryotic phytoplankton typically lack the capacity to utilize phosphonates, certain algal-associated bacteria possess the ability to degrade these compounds. However, no specific strains have been thoroughly examined. Here, we report the discovery of a bacterial strain capable of phosphonate utilization through a specific metabolic pathway. This bacterium was isolated from the dinoflagellate Prorocentrum donghaiense, one of the most prevalent red tide-forming species in China. It can promote the growth of P. donghaiense by supplying phosphate derived from phosphonate degradation. These findings highlight the critical role of bacteria in facilitating phosphonate utilization by dinoflagellates. This mechanism may contribute to the development of harmful algal blooms, which underscores the ecological importance of the algae-bacteria interactions in marine ecosystems.