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

To understand the role of micrometer-scale oxygen (O-2) gradients in facilitating dinitrogen (N-2) fixation, we characterized O-2 dynamics in the microenvironment around free-floating trichomes and colonies of Trichodesmium erythraeum IMS101. Diurnal and spatial variability in O-2 concentrations in the bulk medium, within colonies, along trichomes and within single cells were determined using O-2 optodes, microsensors and model calculations. Carbon (C) and N-2 fixation as well as O-2 evolution and uptake under different O-2 concentrations were analyzed by stable isotope incubations and membrane inlet mass spectrometry. We observed a pronounced diel rhythm in O-2 fluxes, with net O-2 evolution restricted to short periods in the morning and evening, and net O-2 uptake driven by dark respiration and light-dependent O-2 uptake during the major part of the light period. Remarkably, colonies showed lower N-2 fixation and C fixation rates than free-floating trichomes despite the long period of O-2 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 N-2 fixation.