Hydrogen Dynamics in Trichodesmium Colonies and Their Potential Role in Mineral Iron Acquisition

N₂-fixing cyanobacteria mediate H₂ fluxes through the opposing processes of H₂ evolution, which is a by-product of the N₂ fixation reaction, and H₂ uptake, which is driven by uptake hydrogenases. Here, we used microelectrodes to characterize H₂ and O₂ dynamics in single natural colonies of the globally important N₂ fixer Trichodesmium collected from the Gulf of Eilat. We observed gradually changing H₂ dynamics over the course of the day, including both net H₂ evolution and net H₂ uptake, as well as large differences in H₂ fluxes between individual colonies. Net H₂ uptake was observed in colonies amended with H₂ in both light and dark. Net H₂ evolution was recorded in the light only, reflecting light-dependent N₂ fixation coupled to H₂ evolution. Both net H₂ evolution and H₂ uptake rates were higher before 2 pm than later in the day. These pronounced H₂ dynamics in the morning coincided with strong net O₂ uptake and the previously reported diel peak in N₂ fixation. Later in the afternoon, when photosynthesis rates determined by O₂ measurements were highest, and N₂ fixation rates decrease according to previous studies, the H₂ dynamics were also less pronounced. Thus, the observed diel variations in H₂ dynamics reflect diel changes in the rates of O₂ consumption and N₂ fixation. Remarkably, the presence of H₂ 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 N₂-fixing cells, H₂ may contribute to iron uptake in Trichodesmium colonies.