Abstract
Marine nitrogen (N2) fixation was historically considered to be absent or reduced in nitrate (NO3−) rich environments. This is commonly attributed to the lower energetic cost of NO3− uptake compared to diazotrophy in oxic environments. This paradigm often contributes to making inferences about diazotroph distribution and activity in the ocean, and is also often used in biogeochemical ocean models. To assess the general validity of this paradigm beyond the traditionally used model organism Trichodesmium spp., we grew cultures of the unicellular cyanobacterium Crocosphaera watsonii WH8501 long term in medium containing replete concentrations of NO3−. NO3− uptake was measured in comparison to N2 fixation to assess the cultures’ nitrogen source preferences. We further measured culture growth rate, cell stoichiometry, and carbon fixation rate to determine if the presence of NO3− had any effect on cell metabolism. We found that uptake of NO3− by this strain of Crocosphaera was minimal in comparison to other N sources (~2–4% of total uptake). Furthermore, availability of NO3− did not statistically alter N2 fixation rate nor any aspect of cell physiology or metabolism measured (cellular growth rate, cell stoichiometry, cell size, nitrogen fixation rate, nitrogenase activity) in comparison to a NO3− free control culture. These results demonstrate the capability of a marine diazotroph to fix nitrogen and grow independently of NO3−. This lack of sensitivity of diazotrophy to NO3− suggests that assumptions often made about, and model formulations of, N2 fixation should be reconsidered.
Highlights
One of the key parameters classically considered to constrain the distribution of diazotrophs in the ocean is the availability, or lack thereof, of dissolved inorganic nitrogen (DIN)
N2 fixation rates remains an open debate, with evidence pointing to their systematic underestimation
Questionable paradigm suggests that open ocean diazotrophs will not be found fixing nitrogen in areas where NO3 − is available
Summary
One of the key parameters classically considered to constrain the distribution of diazotrophs in the ocean is the availability, or lack thereof, of dissolved inorganic nitrogen (DIN). Two main arguments for this are brought forward in the literature. Nitrate (NO3 − ) has been shown in oxic waters to be less costly than that of nitrogenase activity to convert N2 to NH4 + [1,2,3], and the diel synthesis of the nitrogenase complex imposes additional costs upon diazotrophic cells [2]. One might assume that a diazotroph would, in oxic environments, always choose DIN over N2 whenever available. Marine diazotrophs tend to be slow-growing compared to other phytoplankton, and are not the most efficient in taking up inorganic nutrients [4].
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