Phosphate diester utilization by marine diazotrophs Trichodesmium erythraeum and Crocosphaera watsonii

Abstract

In the phosphate-depleted oligotrophic ocean, microbes utilize various dissolved organic phosphorus (P) compounds as alternative P sources, using enzymes such as alkaline phosphatases. However, knowledge of such P acquisition mechanisms is limited, especially in association with the physiology of nitrogen-fixing organisms, which play a substantial role in marine biogeochemical cycling. We show that nonaxenic clonal cultures of 2 oceanic diazotrophs,Trichodesmium erythraeumandCrocosphaera watsonii, have the ability to utilize phosphate diester as their sole P source, using a model artificial compound—bis-p-nitrophenyl phosphate (bisNPP). Although both diazotroph cultures likely preferred phosphate monoester to diester, the expressed diesterase activity was theoretically sufficient to fulfill their P demands, and they showed significant growth in bisNPP-added media. Interestingly, a distinct difference in their growth trends was observed, with faster onset of growth byC. watsoniiand delayed onset of growth byT. erythraeum. This indicates that theC. watsoniiconsortium can effectively and rapidly assimilatein situdiesters as alternative P sources in the field. Nonetheless, when considering the poor bisNPP utilization reported from other marine phytoplankton taxa, our results indicate that the utilization of particular diester compounds is a notable and advantageous strategy for both diazotroph consortia to alleviate P limitation in the oligotrophic ocean.