Coordinated carbon and nitrogen metabolism in attaining iron homeostasis in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH8501

Abstract

Marine diazotrophic cyanobacteria are ocean's primary producers and suppliers of “new” nitrogen (N) due to their capability to perform both photosynthesis and N₂ fixation, which require iron (Fe)—an extremely scarce trace metal in world's surface ocean—as a cofactor. While enhanced phytoplankton growth as a result of Fe fertilization has been frequently encountered, how marine diazotrophs adjust basal physiology and metabolism in response to varied Fe availability, particularly from a single-cell perspective, remains elusive. Here we show coordinated carbon (C) and N metabolism in sustaining Fe homeostasis in the unicellular N₂-fixing cyanobacterium Crocosphaera watsonii WH8501. Fe deficiency inhibited cell growth, photosynthesis and N₂ fixation, leading to a decrease in the content of particulate organic C and N. However, the C:N ratio in the Fe-deficient cells was significantly higher than that in the Fe-replete cells, coinciding with a greater reduction in metalloenzyme inventory associated with N metabolism than with C metabolism. Intriguingly, Fe deficiency caused C flux toward Fe-independent glycolysis and bypassing the Fe-dependent tricarboxylic acid cycle so that Fe can be reallocated to superoxide dismutase to maintain redox balance. Meanwhile, upregulation of the nitrate/nitrite assimilation enzymes under Fe deficiency further alleviated the high Fe demand of N₂ fixation. Taken together, this study highlights physiological basis underpinning Crocosphaera phenotypic plasticity in regulating central metabolism to acclimatize Fe availability, which is of important reference in assessing marine diazotrophs adaptation to changing marine ecosystem.