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Abstract Increased stratification and mixed layer shoaling of the surface ocean resulting from warming can lead to exposure of marine dinitrogen (N2)‐fixing cyanobacteria to higher levels of inhibitory ultraviolet (UV) radiation. These same processes also reduce vertically advected supplies of the potentially limiting nutrient phosphorus (P) to N2fixers. It is currently unknown how UV inhibition and P limitation interact to affect the biogeochemical cycles of nitrogen and carbon in these biogeochemically critical microbes. We investigated the responses of the important and widespread marine N2‐fixing cyanobacteria
Crocosphaera (strain WH0005) andTrichodesmium (strains IMS 101 and GBR) to UV‐A and UV‐B under P‐replete and P‐limited conditions. Growth, N2fixation, and carbon dioxide (CO2) fixation rates ofTrichodesmium IMS 101 andCrocosphaera were negatively affected by UV exposure. This inhibition was greater forTrichodesmium IMS 101 than forCrocosphaera , which fixes N2only during the night and so avoids direct UV damage. Negative effects of UV on both IMS 101 andCrocosphaera were less in P‐limited cultures than in P‐replete cultures. In contrast, no UV inhibition was observed in GBR, regardless of P availability. UV inhibition was related to different amounts of UV‐absorbing compounds produced by these isolates. Responses to UV radiation and P availability interactions were taxon‐specific, but our results indicated that in general, UV radiation effects onTrichodesmium andCrocosphaera range from negative to neutral. UV inhibition and its interactions with P limitation may thus have a substantial influence on the present day and future nitrogen and carbon cycles of the ocean. -
Gilbert, Jack (Ed.)ABSTRACT The cyanobacterium Trichodesmium is an important contributor of new nitrogen (N) to the surface ocean, but its strategies for protecting the nitrogenase enzyme from inhibition by oxygen (O 2 ) remain poorly understood. We present a dynamic physiological model to evaluate hypothesized conditions that would allow Trichodesmium to carry out its two conflicting metabolic processes of N 2 fixation and photosynthesis. First, the model indicates that managing cellular O 2 to permit N 2 fixation requires high rates of respiratory O 2 consumption. The energetic cost amounts to ∼80% of daily C fixation, comparable to the observed diminution of the growth rate of Trichodesmium relative to other phytoplankton. Second, by forming a trichome of connected cells, Trichodesmium can segregate N 2 fixation from photosynthesis. The transfer of stored C to N-fixing cells fuels the respiratory O 2 consumption that protects nitrogenase, while the reciprocal transfer of newly fixed N to C-fixing cells supports cellular growth. Third, despite Trichodesmium lacking the structural barrier found in heterocystous species, the model predicts low diffusivity of cell membranes, a function that may be explained by the presence of Gram-negative membrane, production of extracellular polysaccharide substances (EPS), and “buffer cells” that intervene between N 2 -fixing and photosynthetic cells. Our results suggest that all three factors—respiratory protection, trichome formation, and diffusion barriers—represent essential strategies that, despite their energetic costs, facilitate the growth of Trichodesmium in the oligotrophic aerobic ocean and permit it to be a major source of new reactive nitrogen. IMPORTANCE Trichodesmium is a major nitrogen-fixing cyanobacterium and exerts a significant influence on the oceanic nitrogen cycle. It is also a widely used model organism in laboratory studies. Since the nitrogen-fixing enzyme nitrogenase is extremely sensitive to oxygen, how these surface-dwelling plankton manage the two conflicting processes of nitrogen fixation and photosynthesis has been a long-standing question. In this study, we developed a simple model of metabolic fluxes of Trichodesmium capturing observed daily cycles of photosynthesis, nitrogen fixation, and boundary layer oxygen concentrations. The model suggests that forming a chain of cells for spatially segregating nitrogen fixation and photosynthesis is essential but not sufficient. It also requires a barrier against oxygen diffusion and high rates of oxygen scavenging by respiration. Finally, the model indicates an extremely short life span of oxygen-enabling cells to instantly create a low-oxygen environment upon deactivation of photosynthesis.more » « less
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Abstract. Trichodesmium is a globally important marine microbe that provides fixednitrogen (N) to otherwise N-limited ecosystems. In nature, nitrogen fixationis likely regulated by iron or phosphate availability, but the extent andinteraction of these controls are unclear. From metaproteomics analysesusing established protein biomarkers for nutrient stress, we foundthat iron–phosphate co-stress is the norm rather than the exception for Trichodesmium colonies in theNorth Atlantic Ocean. Counterintuitively, the nitrogenase enzyme was moreabundant under co-stress as opposed to single nutrient stress. This isconsistent with the idea that Trichodesmium has a specific physiological state duringnutrient co-stress. Organic nitrogen uptake was observed and occurredsimultaneously with nitrogen fixation. The quantification of the phosphate ABCtransporter PstA combined with a cellular model of nutrient uptake suggestedthat Trichodesmium is generally confronted by the biophysical limits of membrane spaceand diffusion rates for iron and phosphate acquisition in the field. Colonyformation may benefit nutrient acquisition from particulate and organicsources, alleviating these pressures. The results highlight that topredict the behavior of Trichodesmium, both Fe and P stress must be evaluatedsimultaneously.more » « less
