N₂ fixation in free-floating filaments of Trichodesmium is higher than in transiently suboxic colony...

To understand the role of micrometer-scale oxygen (O₂ ) gradients in facilitating dinitrogen (N₂ ) fixation, we characterized O₂ dynamics in the microenvironment around free-floating trichomes and colonies of Trichodesmium erythraeum IMS101. Diurnal and spatial variability in O₂ concentrations in the bulk medium, within colonies, along trichomes and within single cells were determined using O₂ optodes, microsensors and model calculations. Carbon (C) and N₂ fixation as well as O₂ evolution and uptake under different O₂ concentrations were analyzed by stable isotope incubations and membrane inlet mass spectrometry. We observed a pronounced diel rhythm in O₂ fluxes, with net O₂ evolution restricted to short periods in the morning and evening, and net O₂ uptake driven by dark respiration and light-dependent O₂ uptake during the major part of the light period. Remarkably, colonies showed lower N₂ fixation and C fixation rates than free-floating trichomes despite the long period of O₂ undersaturation in the colony microenvironment. Model calculations demonstrate that low permeability of the cell wall in combination with metabolic heterogeneity between single cells allows for anoxic intracellular conditions in colonies but also free-floating trichomes of Trichodesmium. Therefore, whereas colony formation must have benefits for Trichodesmium, it does not favor N₂ fixation.