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 (NO3-). 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 (mu) was limited by low light (mu=0.23 d(-1)), short-term experiments indicated that 0.4 mu M NH4+ reduced N-2-fixation by similar to 90% relative to controls without added NH4+. In fast-growing, high-light-acclimated cultures (mu=0.68 d(-1)), 2.0 mu M NH4+ was needed to achieve the same effect. In long-term exposures to NO3-, inhibition of N-2 fixation also varied with growth rate. In high-light-acclimated, fast-growing cultures, NO3- did not inhibit N-2-fixation rates in comparison with cultures growing on N-2 alone. Instead NO3- 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, NO3- 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.