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

Abstract

Biological N2 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 N2 fixation is uncertain. Thus, global estimates of new oceanic N depend on a fundamental understanding of factors that modulate N source preferences by N2-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 N2 fixation. When growth (µ) was limited by low light (µ = 0.23 d−1), short-term experiments indicated that 0.4 µM NH4 + reduced N2-fixation by ∼90% relative to controls without added NH4 +. In fast-growing, high-light-acclimated cultures (µ = 0.68 d−1), 2.0 µM NH4 + was needed to achieve the same effect. In long-term exposures to NO3 −, inhibition of N2 fixation also varied with growth rate. In high-light-acclimated, fast-growing cultures, NO3 − did not inhibit N2-fixation rates in comparison with cultures growing on N2 alone. Instead NO3 − supported even faster growth, indicating that the cellular assimilation rate of N2 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 N2-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 N2 fixation by fixed N sources based on the growth rate as controlled by light.

Dimensions of marine phytoplankton diversity

“…Additional data are derived from separate measurement of size and growth: these are shown as light lines centred at the mean and arms covering range. These are for the pico-prokaryotes (green) Prochlorococcus and Synechococcus (Morel et al, 1993;Johnson et al, 2006;Christaki et al, 1999;Moore et al, 1998;Agawin and Agustí, 1997) and the diazotrophs (light blue) Crocosphaera and Trichodesmium (Garcia and Hutchins, 2014;Webb et al, 2009;Wilson et al, 2017;Bergman et al, 2013;Boatman et al, 2017;Breitbarth et al, 2008;Hutchins et al, 2007;Kranz et al, 2010;Shi et al, 2012). of group-specific accessory pigments) and scattering of light. The absorption spectra are flatter with larger sizes following Finkel and Irwin (2000) to account for self-shading, and scattering spectra are also influenced by size following Stramski et al (2001) (see Text S1.3, Fig.…”

“…The simulation uses Monod kinetics, and C : N : P : Fe stoichiometry is constant over time (though it differs between phytoplankton groups). Chl a for each phytoplankton type varies in time and space depending on light, nutrient and temperature conditions following Geider et al (1998). Following empirical evidence, mixotrophic dinoflagellates are assumed to have lower maximum photosynthetic growth rates than other phytoplankton of the same size (Tang, 1995;Fig.…”

Dimensions of Marine Phytoplankton Diversity

“…Additional data are derived from separate measurement of size and growth: These are shown as light lines centered at the mean and arms covering range. These are for the pico-prokaryotes (green) Prochlorococcus and Synecochoccus (Morel et al, 1993, Johnson et al 2006, Christaki et al 1999, Moore et al 1998, Agawin and Agustí 1997 and the diazotrophs (light blue) Crocosphera and Trichodesmium (Garcia and Hutchins, 2014;Webb et al, 2009;Wilson et al, 2017;Bergman et al, 2013;Boatman et al 2017;Beithbarth et al, 2008;Hutchins et al 2007;Kranz et al, 2010;Shi et al, 2012). Figure 11: Sensitivity simulations, model annual mean richness for trait dimensions.…”

Two subpopulations of Crocosphaera watsonii have distinct distributions in the North and South Pacific

“…The negative correlation with ammonia may be an indication of the type of N 2 ‐fixation inhibition by ammonia that was observed in Crocosphaera culture experiments (Dekaezemacker and Bonnet, ; Garcia and Hutchins, ). Those studies found that the effect of N 2 ‐fixation inhibition was stronger under low light growth conditions (Garcia and Hutchins, ) and also stronger in large cell strains compared with small cell strains (Dekaezemacker and Bonnet, ). Given those results, it is notable that there was a dominance of large cells in deeper water where ammonia concentrations are higher and light levels are lower.…”