Co-acquisition of mineral-bound iron and phosphorus by natural Trichodesmium colonies

Low iron (Fe) and phosphorus (P) ocean regions are often home to the globally important N-2-fixing cyanobacterium Trichodesmium spp., which are physiologically adapted to Fe/P co-limitation. Given Trichodesmium's eminent ability to capture particles and the common associations between Fe and P in sediments and aerosols, we hypothesized that mineral bio-dissolution by Trichodesmium spp. may enable them to co-acquire Fe and P. We present a new sensitive assay to determine P uptake from particles, utilizing P-33-labeled ferrihydrite. To validate the method, we examined single natural Trichodesmium thiebautii colonies in a high-resolution radiotracer ss-imager, identifying strong colony-mineral interactions, efficient removal of external P-33-labeled ferrihydrite, and elevated P-33 uptake in the colony core. Next, we determined bulk P uptake rates, comparing natural Red Sea colonies and P-limited Trichodesmium erythraeum cultures. Uptake rates by natural and cultured Trichodesmium were similar to P release rates from the mineral, suggesting tight coupling between dissolution and uptake. Finally, synthesizing P-ferrihydrite labeled with either P-33 or Fe-55, we probed for Fe/P co-extraction by common microbial mineral solubilization pathways. Dissolution rates of ferrihydrite were accelerated by exogenous superoxide and strong Fe-chelator and subsequently enhanced P-33 release and uptake by Trichodesmium. Our method and findings can facilitate further Fe/P co-acquisition studies and highlight the importance of biological mechanisms and microenvironments in controlling bioavailability and nutrient fluxes from particles.