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Inomura, K.

Publications and source records attributed to Inomura, K..

6 recordsLinked to original sources

Cellular-level control on global ocean deoxygenation driven by phytoplankton ecophysiology

Phytoplankton elemental composition shapes the distribution of dissolved nutrient concentrations and thus plays a key role in ocean biogeochemistry. While the carbon-to-nitrogen-to-phosphorus ratio (C:N:P) in marine phytoplankton has been extensively studied, the hydrogen (H) and oxygen (O) content have received less attention despite their critical role in determining dissolved oxygen (O2) consumption rates in the ocean. Here, we estimated the elemental composition of marine phytoplankton, including the H and O content, from first principles, using a cellular allocation model embedded in a global ocean model. We estimated that an average phytoplankton cell has a chemical formula of C107H190N16O53P, with an O2 demand of 149 mol O2/mol P and respiration quotients of 1.40 mol O2/mol C, suggesting a lower H and O content, and higher O2 demand than commonly assumed. We found global variations in the O2 demand of organic matter respiration driven by population structure and cellular reorganisation under different environmental conditions. By testing how shifts in the macromolecular composition of phytoplankton cells affect the oceans O2 budget, we found that O2 consumption increases significantly when shifting cell composition from carbohydrate-rich to protein- or lipid-rich cells. As a result, low-O2 (hypoxic) zones in the ocean expanded by 75%. These findings demonstrate that cellular-level processes in marine phytoplankton shape the global O2 cycle and large-scale patterns of ocean biogeochemistry.

ecology↗

Temporal regulation of metabolic processes in the marine diazotroph Crocosphaera watsonii WH 8501

Marine diazotrophic cyanobacteria play a crucial role in oceanic nitrogen cycling, supporting primary production and ecosystem balance. Crocosphaera watsonii WH8501 exemplifies this ability by temporally separating photosynthesis and diazotrophy to sustain metabolism. To investigate the regulatory mechanisms underlying this process, we employed LC/MS-MS proteomics in a diel culturing experiment, revealing tightly coordinated protein abundance patterns. Our findings showed a sophisticated temporal regulation of metabolic processes categorized within six distinct protein abundance clusters: (1) nitrogen fixation and amino acid biosynthesis proteins peaked during the night, while (2) glycogen metabolism and dark reactions of photosynthesis were most abundant during the night and day-night transition, likely supporting carbon consumption and energy production. Midday (3 and 4) was dominated by proteins related to photosynthesis, cellular division, and lipid synthesis, whereas late-day peaks (5) in peptide biosynthesis may facilitate nitrogenase complex formation. Notably, the day-night transition (6) exhibited fine-tuned coordination of nitrogenase assembly, with FeS cluster proteins preceding peak nitrogenase iron protein abundance, implying a temporally ordered sequence for functional enzyme formation. Within these categories, sharp temporal patterns emerged in iron trafficking to heme and iron cluster biosynthetic systems, consistent with the need to maintain tight control of iron distribution to metalloproteins at each temporal transition. These results highlight the intricate diel regulation that enables Crocosphaera to balance nitrogen fixation and photosynthesis within a single cell. The observed coordination supports the existence of a complex regulatory system ensuring optimal metabolic performance, reinforcing the critical role of temporal control in sustaining these globally significant biological processes.

microbiology↗

Modeling dynamic oxygen permeability as a mechanism to mitigate oxygen-induced stresses on photosynthesis and N2 fixation in marine Trichodesmium

Trichodesmium, the predominant marine diazotrophic cyanobacterium, concurrently performs nitrogen (N2) fixation and photosynthesis, the latter of which produces oxygen (O2) that inhibits N2 fixation. Hopanoid lipids in Trichodesmium may play a role in dynamically regulating membrane permeability to O2, potentially alleviating O2 stress on N2 fixation. However, the physiological impacts of this dynamic permeability are not well understood. We developed a model showing that dynamically modulating membrane O2 permeability can enhance N2 fixation and growth of Trichodesmium by over 50%. High O2 permeability (1.5x10-4 of O2 diffusivity in seawater) during strong photosynthesis accelerates O2 exhaust, reducing energy-consuming photorespiration by [~]40%, while low O2 permeability (1.0x10-5 diffusivity) during active N2 fixation minimizes O2 stress on N2 fixation. Together, these mechanisms increase the carbon and iron use efficiencies by [~]70%. Our study provides a mechanistic and quantitative framework for how dynamic O2 permeability benefits Trichodesmium, offering insights potentially applicable to other diazotrophs. IMPORTANCETrichodesmium is a key player in marine N2 fixation, essential for oceanic productivity and global biogeochemical cycles. However, a significant challenge arises from the concurrent photosynthetic production of O2 during N2 fixation, which can inhibit N2 fixation and cause energy-wasting photorespiration. We develop a physiological model showing that Trichodesmium may dynamically regulate membrane O2 permeability to enhance N2 fixation and growth. The model suggests two mechanisms: elevated O2 permeability during the early daytime of strong photosynthesis accelerates O2 exhaust to environment, reducing photorespiration, while reduced O2 permeability later limits O2 influx from environment, lowering wasteful respiration and maintaining a low intracellular O2 level for active N2 fixation. These adaptations improve the efficiency of carbon and iron utilization, thereby facilitating N2 fixation and growth in Trichodesmium. This study sheds light on how Trichodesmium and other N2-fixing microorganisms can optimize their physiological processes in response to environmental challenges. HIGHLIGHTSO_LIWe developed a metabolic flux model of Trichodesmium, which resolves Dynamic cellular Permeability to O2 (DPO2). C_LIO_LIDPO2 increases N2 fixation and growth rates. C_LIO_LIDPO2 increases growth efficiency by reducing carbon wasting processes such as photorespiration and respiratory protection. C_LIO_LIDPO2, as a result, also increases iron utilization efficiency. C_LI

microbiology↗

Rapid mode switching facilitates the growth of Trichodesmium: A model analysis.

Trichodesmium is one of the dominant dinitrogen(N2)-fixers in the ocean, influencing global carbon and nitrogen cycles through its biochemical reactions. Although the photosynthetic activity of Trichodesmium fluctuates rapidly at the cellular level, the physiological or ecological advantage of this characteristic is not clear. Here we develop a metabolic model of Trichodesmium that can perform dinitrogen (N2) fixation during the daytime. We examined (1) the effect of the duration of switches between photosynthetic and non-photosynthetic cellular states and (2) the effect of the presence and absence of N2 fixation in photosynthetic states. Our results show that a rapid switch between photosynthetic and non-photosynthetic states increases Trichodesmium growth rates by improving metabolic efficiencies due to optimized C and N metabolism. Our results show the possibility and advantage of the rapid switch, providing a strategy for previous observations that all Trichodesmium cells can contain nitrogenase, which was previously considered to be a paradox. This study reveals the importance of fluctuating photosynthetic activity and provides a mechanism for daytime N2 fixation that allows Trichodesmium to fix N2 aerobically in the global ocean.

ecology↗

Proton-pumping rhodopsins in marine diatoms

Diatoms are a major phytoplankton group responsible for about 20% of Earths primary production. They carry out photosynthesis inside the plastid, an organelle obtained through eukaryote-eukaryote endosymbiosis. Recently, microbial rhodopsin, a photoreceptor distinct from chlorophyll-based photosystems, has been identified in certain diatoms. However, the physiological function of diatom rhodopsin is not well understood. Here we show that the diatom rhodopsin acts as a light-driven proton pump and localizes to the outermost membrane of the four membrane-bound complex plastids. Heterologous expression techniques were used to investigate the protein function and subcellular localization of diatom rhodopsin. Using model simulations, we further evaluated the physiological role of the acidic pool in the plastid produced by proton-transporting rhodopsin. Our results propose that the rhodopsin-derived acidic pool may be involved in a photosynthetic CO2-concentrating mechanism and assist CO2 fixation in diatom cells.

microbiology↗

Crocosphaera as a major consumer of fixed nitrogen despite its capability of nitrogen fixation

Crocosphaera watsonii (hereafter Crocosphaera) is a key nitrogen (N) fixer in the ocean, but its ability to consume combined N sources is still unclear. Using in situ microcosm incubations with an ecological model, we show that Crocosphaera has high competitive capability both under low and moderately high combined N concentrations. In field incubations, Crocosphaera accounted for the highest consumption of ammonium and nitrate, followed by pico-eukaryotes. The model analysis shows that cells have a high ammonium uptake rate ([~]7 mol N (mol N)-1 d-1 at the maximum), which allows them to compete against pico-eukaryotes and non-diazotrophic cyanobacteria when combined N is sufficiently available. Even when combined N is depleted, their capability of nitrogen fixation allows higher growth rates compared to potential competitors. These results suggest the high fitness of Crocosphaera in combined N limiting, oligotrophic oceans, and thus heightens its potential significance in its ecosystem and in biogeochemical cycling.

microbiology↗