Multiple Phosphonate Degradation Pathways in Amphidinium carterae-Associated Bacteria Potentially Contribute to Host Adaptation to Phosphorus Limitation

Phosphonates in the ocean can serve as an alternative phosphorus (P) source for microorganisms when phosphate is scarce. Dinoflagellates cannot utilize phosphonates, but some associated bacteria can degrade these compounds and release phosphate. However, the community composition of these bacteria and their phosphonate degradation pathways remain poorly understood. In this study, the dinoflagellate Amphidinium carterae was cultured with 2-aminoethylphosphonic acid (2-AEP) as the exclusive P source. Metagenomic and genomic analyses were conducted to identify bacterial taxa and genes related to phosphonate utilization (phn genes). Specific strains were isolated from 2-AEP cultures to characterize phosphonate degradation gene clusters. Ten of the 20 most abundant genera were found to possess the genetic potential for phosphonate utilization, with Labrenzia, Phycocomes, and Pseudosulfitobacter as the dominant genera. The identified phn genes constituted multiple pathways, including the C-P lyase, PhnW-PhnX, and PhnW-PhnY-PhnA pathways, indicating that A. carterae-associated bacteria can utilize phosphonates through diverse mechanisms, with some strains even possessing more than one pathway. Five isolated bacterial strains were confirmed to be capable of degrading 2-AEP. These findings underscore the ecological significance of bacterial diversity and metabolic versatility in helping dinoflagellate hosts adapt to P scarcity, providing novel insights into bacteria-algae interactions and marine P cycling.