Trichodesmium, a globally important, N 2 -fixing, and colony-forming cyanobacterium, employs multiple pathways for acquiring nutrients from air-borne dust, including active dust collection. Once concentrated within the colony core, dust can supply Trichodesmium with nutrients. Recently, we reported a selectivity in particle collection enabling Trichodesmium to center iron-rich minerals and optimize its nutrient utilization. In this follow-up study we examined if colonies select Phosphorus (P) minerals. We incubated 1,200 Trichodesmium colonies from the Red Sea with P-free CaCO 3 , P-coated CaCO 3 , and dust, over an entire bloom season. These colonies preferably interacted, centered, and retained P-coated CaCO 3 compared with P-free CaCO 3 . In both studies, Trichodesmium clearly favored dust over all other particles tested, whereas nutrient-free particles were barely collected or retained, indicating that the colonies sense the particle composition and preferably collect nutrient-rich particles. This unique ability contributes to Trichodesmium's current ecological success and may assist it to flourish in future warmer oceans.

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 33 P-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 33 P-labeled ferrihydrite, and elevated 33 P 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 33 P or 55 Fe, 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 33 P 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.

The bloom forming Trichodesmium are filamentous cyanobacteria of key interest due to their ability to fix carbon and nitrogen within an oligotrophic marine environment. Trichodesmium blooms typically comprise a complex assemblage of subpopulations and colony-morphologies that are predicted to exhibit distinct ecological lifestyles. Here, we assessed the poorly studied diversity of Trichodesmium in the Red Sea, based on metagenome-assembled genomes (MAGs) and hetR gene-based phylotyping. We assembled four non-redundant MAGs from morphologically distinct Trichodesmium colonies (tufts, dense and thin puffs). T. thiebautii (puffs) and T. erythraeum (tufts) were the dominant species within these morphotypes. While subspecies diversity is present for both T. thiebautii and T. erythraeum, a single T. thiebautii genotype comprised both thin and dense puff morphotypes, and we therefore hypothesize that the phenotypic variation between these morphologies is likely attributed to gene regulation. Additionally, we found the rare non-diazotrophic clade IV and V genotypes, related to T. nobis and T. miru respectively, that likely occurred as single filaments. HetR gene phylogeny indicates that the genotype in clade IV could represent the species T. contortum. We further show that hetR phylotyping can overestimate the taxonomic diversity of Trichodesmium, as two copies of the hetR gene were present within T. thiebautii genomes, one of which misidentified this lineage as T. aureum. Taken together, our results highlight the importance of re-assessing Trichodesmium taxonomy while showing the ability of genomics to capture the complex diversity and distribution of Trichodesmium populations.