Light-Limited Growth Rate Modulates Nitrate Inhibition of Dinitrogen Fixation in the Marine Unicellular Cyanobacterium Crocosphaera watsonii

Biological N(2) fixation is the dominant supply of new nitrogen (N) to the oceans, but is often inhibited in the presence of fixed N sources such as nitrate (NO(3) (−)). Anthropogenic fixed N inputs to the ocean are increasing, but their effect on marine N(2) fixation is uncertain. Thus, global estimates of new oceanic N depend on a fundamental understanding of factors that modulate N source preferences by N(2)-fixing cyanobacteria. We examined the unicellular diazotroph Crocosphaera watsonii (strain WH0003) to determine how the light-limited growth rate influences the inhibitory effects of fixed N on N(2) fixation. When growth (µ) was limited by low light (µ = 0.23 d(−1)), short-term experiments indicated that 0.4 µM NH(4) (+) reduced N(2)-fixation by ∼90% relative to controls without added NH(4) (+). In fast-growing, high-light-acclimated cultures (µ = 0.68 d(−1)), 2.0 µM NH(4) (+) was needed to achieve the same effect. In long-term exposures to NO(3) (−), inhibition of N(2) fixation also varied with growth rate. In high-light-acclimated, fast-growing cultures, NO(3) (−) did not inhibit N(2)-fixation rates in comparison with cultures growing on N(2) alone. Instead NO(3) (−) supported even faster growth, indicating that the cellular assimilation rate of N(2) alone (i.e. dinitrogen reduction) could not support the light-specific maximum growth rate of Crocosphaera. When growth was severely light-limited, NO(3) (−) did not support faster growth rates but instead inhibited N(2)-fixation rates by 55% relative to controls. These data rest on the basic tenet that light energy is the driver of photoautotrophic growth while various nutrient substrates serve as supports. Our findings provide a novel conceptual framework to examine interactions between N source preferences and predict degrees of inhibition of N(2) fixation by fixed N sources based on the growth rate as controlled by light.