Dataset Information

N₂ fixation in free-floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments.

ABSTRACT: To understand the role of micrometer-scale oxygen (O₂ ) gradients in facilitating dinitrogen (N₂ ) fixation, we characterized O₂ dynamics in the microenvironment around free-floating trichomes and colonies of Trichodesmium erythraeum IMS101. Diurnal and spatial variability in O₂ concentrations in the bulk medium, within colonies, along trichomes and within single cells were determined using O₂ optodes, microsensors and model calculations. Carbon (C) and N₂ fixation as well as O₂ evolution and uptake under different O₂ concentrations were analyzed by stable isotope incubations and membrane inlet mass spectrometry. We observed a pronounced diel rhythm in O₂ fluxes, with net O₂ evolution restricted to short periods in the morning and evening, and net O₂ uptake driven by dark respiration and light-dependent O₂ uptake during the major part of the light period. Remarkably, colonies showed lower N₂ fixation and C fixation rates than free-floating trichomes despite the long period of O₂ undersaturation in the colony microenvironment. Model calculations demonstrate that low permeability of the cell wall in combination with metabolic heterogeneity between single cells allows for anoxic intracellular conditions in colonies but also free-floating trichomes of Trichodesmium. Therefore, whereas colony formation must have benefits for Trichodesmium, it does not favor N₂ fixation.

SUBMITTER: Eichner M

PROVIDER: S-EPMC6590460 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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N2 fixation in free-floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments.

Eichner Meri M Thoms Silke S Rost Björn B Mohr Wiebke W Ahmerkamp Soeren S Ploug Helle H Kuypers Marcel M M MMM de Beer Dirk D

The New phytologist 20181229 2

To understand the role of micrometer-scale oxygen (O2 ) gradients in facilitating dinitrogen (N2 ) fixation, we characterized O2 dynamics in the microenvironment around free-floating trichomes and colonies of Trichodesmium erythraeum IMS101. Diurnal and spatial variability in O2 concentrations in the bulk medium, within colonies, along trichomes and within single cells were determined using O2 optodes, microsensors and model calculations. Ca ...[more]

PMID: 30507001

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Project description:The dominant marine filamentous N2 fixer, Trichodesmium, conducts photosynthesis and N2 fixation during the daytime. Because N2 fixation is sensitive to O2, some previous studies suggested that spatial segregation of N2 fixation and photosynthesis is essential in Trichodesmium. However, this hypothesis conflicts with some observations where all the cells contain both photosystems and the N2-fixing enzyme nitrogenase. Here, we construct a systematic model simulating Trichodesmium metabolism, showing that the hypothetical spatial segregation is probably useless in increasing the Trichodesmium growth and N2 fixation, unless substances can efficiently transfer among cells with low loss to the environment. The model suggests that Trichodesmium accumulates fixed carbon in the morning and uses that in respiratory protection to reduce intracellular O2 during the mid-daytime, when photosynthesis is downregulated, allowing the occurrence of N2 fixation. A cell membrane barrier against O2 and alternative non-O2 evolving electron transfer also contribute to maintaining low intracellular O2. Our study provides a mechanism enabling N2 fixation despite the presence of photosynthesis across Trichodesmium. IMPORTANCE The filamentous Trichodesmium is a globally prominent marine nitrogen fixer. A long-standing paradox is that the nitrogen-fixing enzyme nitrogenase is sensitive to oxygen, but Trichodesmium conducts both nitrogen fixation and oxygen-evolving photosynthesis during the daytime. Previous studies using immunoassays reported that nitrogenase was limited in some specialized Trichodesmium cells (termed diazocytes), suggesting the necessity of spatial segregation of nitrogen fixation and photosynthesis. However, attempts using other methods failed to find diazocytes in Trichodesmium, causing controversy on the existence of the spatial segregation. Here, our physiological model shows that Trichodesmium can maintain low intracellular O2 in mid-daytime and achieve feasible nitrogen fixation and growth rates even without the spatial segregation, while the hypothetical spatial segregation might not be useful if substantial loss of substances to the environment occurs when they transfer among the Trichodesmium cells. Our study then suggests a possible mechanism by which Trichodesmium can survive without the spatial segregation.

Project description:There is considerable debate about the benefits and trade-offs for colony formation in a major marine nitrogen fixer, Trichodesmium. To quantitatively analyze the trade-offs, we developed a metabolic model based on carbon fluxes to compare the performance of Trichodesmium colonies and free trichomes under different scenarios. Despite reported reductions in carbon fixation and nitrogen fixation rates for colonies relative to free trichomes, we found that model colonies can outperform individual cells in several cases. The formation of colonies can be advantageous when respiration rates account for a high proportion of the carbon fixation rate. Negative external influence on vital rates, such as mortality due to predation or micronutrient limitations, can also create a net benefit for colony formation relative to individual cells. In contrast, free trichomes also outcompete colonies in many scenarios, such as when respiration rates are equal for both colonies and individual cells or when there is a net positive external influence on rate processes (i.e., optimal environmental conditions regarding light and temperature or high nutrient availability). For both colonies and free trichomes, an increase in carbon fixation relative to nitrogen fixation rates would increase their relative competitiveness. These findings suggest that the formation of colonies in Trichodesmium might be linked to specific environmental and ecological circumstances. Our results provide a road map for empirical studies and models to evaluate the conditions under which colony formation in marine phytoplankton can be sustained in the natural environment. IMPORTANCETrichodesmium is a marine filamentous cyanobacterium that fixes nitrogen and is an important contributor to the global nitrogen cycle. In the natural environment, Trichodesmium can exist as individual cells (trichomes) or as colonies (puffs and tufts). In this paper, we try to answer a longstanding question in marine microbial ecology: how does colony formation benefit the survival of Trichodesmium? To answer this question, we developed a carbon flux model that utilizes existing published rates to evaluate whether and when colony formation can be sustained. Enhanced respiration rates, influential external factors such as environmental conditions and ecological interactions, and variable carbon and nitrogen fixation rates can all create scenarios for colony formation to be a viable strategy. Our results show that colony formation is an ecologically beneficial strategy under specific conditions, enabling Trichodesmium to be a globally significant organism.

Dataset Information

N₂ fixation in free-floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments.

Publications

N<sub>2</sub> fixation in free-floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments.

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