In the last decade, the northern Arabian Sea has witnessed a radical shift in the composition of winter phytoplankton blooms, which previously comprised mainly of diatoms, the unicellular, siliceous photosynthetic organisms favoured by nutrient-enriched waters from convective mixing. These trophically important diatom blooms have been replaced by widespread blooms of a large, green dinoflagellate, Noctiluca scintillans, which combines carbon fixation from its chlorophyll-containing endosymbiont with ingestion of prey. Here, we report that these massive outbreaks of N. scintillans during winter are being facilitated by an unprecedented influx of oxygen deficient waters into the euphotic zone and by the extraordinary ability of its endosymbiont Pedinomonas noctilucae to fix carbon more efficiently than other phytoplankton under hypoxic conditions. We contend that N. scintillans blooms could disrupt the traditional diatom-sustained food chain to the detriment of regional fisheries and long-term health of an ecosystem supporting a coastal population of nearly 120 million people.

Iron (Fe) bioavailability limits phytoplankton growth in vast ocean regions. Iron-rich dust uplifted from deserts is transported in the atmosphere and deposited on the ocean surface. However, this dust is a poor source of iron for most phytoplankton since dust-bound Fe is poorly soluble in seawater and dust rapidly sinks out of the photic zone. An exception is Trichodesmium , a globally important, N 2 fixing, colony forming, cyanobacterium, which efficiently captures and shuffles dust to its colony core. Trichodesmium and bacteria that reside within its colonies carry out diverse metabolic interactions. Here we show evidence for mutualistic interactions between Trichodesmium and associated bacteria for utilization of iron from dust, where bacteria promote dust dissolution by producing Fe-complexing molecules (siderophores) and Trichodesmium provides dust and optimal physical settings for dissolution and uptake. Our results demonstrate how intricate relationships between producers and consumers can influence productivity in the nutrient starved open ocean.

The high iron (Fe) demands of Trichodesmium, a keystone nitrogen‐fixing cyanobacterium, are often met by dust deposition at the ocean surface. Following up on our findings of unique dust capturing and processing by Trichodesmium, we explored the ability of natural Trichodesmium colonies from the Gulf of Aqaba and Fe‐limited laboratory culture (IMS101) to obtain Fe from the mineral ferrihydrite and compete with their epibiotic bacteria for this Fe source. To study this complex system, we carefully optimized a radiotracer method ensuring complete removal of external ferrihydrite and efficient separation of bacteria from the colonies. Trichodesmium‐only uptake rates of natural colonies were 5–50 times faster than those of laboratory culture, suggesting that natural colonies acquire ferrihydrite at a greater efficiency. In some days, total uptake rates of natural colonies exceeded dissolved Fe release from ferrihydrite, indicating that the colonies enhance the mineral dissolution rate. Furthermore, uptake rates of bacteria associated with natural colonies were faster than those of bacteria associated with the culture, implying that the bacteria benefit from the Trichodesmium‐enhanced mineral dissolution. At the cellular level, surface area normalized uptake rates of bacteria always exceeded those of cultured Trichodesmium, but in natural populations, the dominance shifted between Trichodesmium and bacteria on different days. At the community level, when accounting for the total bacteria and Trichodesmium cells, Trichodesmium dominated Fe uptake in both cultured and natural colonies. Overall, our findings suggest that natural Trichodesmium colonies are exceptionally adapted for accessing mineral Fe and maintaining a sustainable relationship with their associated bacteria.

Dust is an important iron (Fe) source to the ocean, but its utilization by phytoplankton is constrained by rapid sinking and slow dissolution dust-bound iron (dust-Fe). Colonies of the globally important cyanobacterium, Trichodesmium, overcome these constraints by efficient dust capturing and active dust-Fe dissolution. In this study we examined the ability of Trichodesmium colonies to maximize their Fe supply from dust by selectively collecting Fe-rich particles. Testing for selectivity in particle collection, we supplied ~600 individual colonies, collected on multiple days from the Gulf of Aqaba, with natural dust and silica minerals that were either cleaned of or coated with Fe. Using a stereoscope, we counted the number of particles retained by each colony shortly after addition and following 24 h incubation with particles, and documented translocation of particles to the colony core. We observed a strong preference for Fe-rich particles over Fe-free particles in all tested parameters. Moreover, some colonies discarded the Fe-free particles they initially collected. The preferred collection of Fe-rich particles and disposal of Fe-free particles suggest that Trichodesmium can sense Fe and selectively choose Fe-rich dust particles. This ability assists Trichodesmium obtain Fe from dust and facilitate its growth and subsequent contribution to nutrient cycling and productivity in the ocean.

Colonies of the marine diazotroph Trichodesmium host a complex microbial population. We show that colony consortia produce metallophores that likely influence the bioavailability of the trace nutrient iron within the colony microenvironment.

N 2 -fixing cyanobacteria mediate H 2 fluxes through the opposing processes of H 2 evolution, which is a by-product of the N 2 fixation reaction, and H 2 uptake, which is driven by uptake hydrogenases. Here, we used microelectrodes to characterize H 2 and O 2 dynamics in single natural colonies of the globally important N 2 fixer Trichodesmium collected from the Gulf of Eilat. We observed gradually changing H 2 dynamics over the course of the day, including both net H 2 evolution and net H 2 uptake, as well as large differences in H 2 fluxes between individual colonies. Net H 2 uptake was observed in colonies amended with H 2 in both light and dark. Net H 2 evolution was recorded in the light only, reflecting light-dependent N 2 fixation coupled to H 2 evolution. Both net H 2 evolution and H 2 uptake rates were higher before 2 pm than later in the day. These pronounced H 2 dynamics in the morning coincided with strong net O 2 uptake and the previously reported diel peak in N 2 fixation. Later in the afternoon, when photosynthesis rates determined by O 2 measurements were highest, and N 2 fixation rates decrease according to previous studies, the H 2 dynamics were also less pronounced. Thus, the observed diel variations in H 2 dynamics reflect diel changes in the rates of O 2 consumption and N 2 fixation. Remarkably, the presence of H 2 strongly stimulated the uptake of mineral iron by natural colonies. The magnitude of this effect was dependent on the time of day, with the strongest response in incubations that started before 2 pm, i.e., the period that covered the time of highest uptake hydrogenase activity. Based on these findings, we propose that by providing an electron source for mineral iron reduction in N 2 -fixing cells, H 2 may contribute to iron uptake in Trichodesmium colonies.

Trichodesmium are filamentous cyanobacteria of key interest due to their ability to fix carbon and nitrogen within an oligotrophic marine environment. Their blooms consist of a dynamic assemblage of subpopulations and colony morphologies that are hypothesized to occupy unique niches. 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). Trichodesmium thiebautii (puffs) and Trichodesmium 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 hypothesize that this phenotypic variation is likely attributed to gene regulation. Additionally, we found the rare non-diazotrophic clade IV and V genotypes, related to Trichodesmium nobis and Trichodesmium miru, respectively that likely occurred as single filaments. The hetR gene phylogeny further indicated that the genotype in clade IV could represent the species Trichodesmium contortum. Importantly, we show the presence of hetR paralogs in Trichodesmium, where two copies of the hetR gene were present within T. thiebautii genomes. This may lead to the overestimation of Trichodesmium diversity as one of the copies misidentified T. thiebautii as Trichodesmium 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.

Colonies of the N2‐fixing cyanobacterium Trichodesmium can harbor distinct chemical microenvironments that may assist the colonies in acquiring mineral iron from dust. Here, we characterized O2 and pH gradients in and around Trichodesmium colonies by microsensor measurements on > 170 colonies collected in the Gulf of Eilat over ∼ 2 months. O2 concentrations and pH values in the center of single colonies decreased in the dark due to respiration, reaching minimum values of 70 μmol L−1 and 7.7, whereas in the light, O2 and pH increased due to photosynthesis, reaching maximum values of 410 μmol L−1 and 8.6. Addition of dust and bacteria and increasing colony size influenced O2 and pH levels in the colonies, yet values remained within the range observed in single natural colonies. However, lower values down to 60 μmol L−1 O2 and pH 7.5 were recorded in the dark in dense surface accumulations of Trichodesmium. Using radiolabelled ferrihydrite, we examined the effect of these conditions on mineral iron dissolution and availability to Trichodesmium. Dark‐incubated colonies did not acquire iron from ferrihydrite faster than light‐incubated colonies, indicating that the dark‐induced decrease in pH and O2 within single colonies is too small to significantly increase mineral iron bioavailability. Yet, ligand‐promoted dissolution of ferrihydrite, a mechanism likely applied by Trichodesmum for acquiring mineral iron, did increase at the lower pH levels observed in surface accumulations. Thus, Trichodesmium surface blooms in their final stage may harbor chemical conditions that enhance the dissolution and bioavailability of mineral iron to the associated microbial community.