Saturating growth rate against phosphorus concentration explained by macromolecular allocation.

IMPORTANCE: The Monod equation has been used to represent the relationship between growth rate and the environmental nutrient concentration under the limitation of this respective nutrient. This model often serves as a means to connect microorganisms to their environment, specifically in ecosystem and global models. Here, we use a simple model of a marine microorganism cell to illustrate the model's ability to capture the same relationship as Monod, while highlighting the additional physiological details our model provides. In this study, we focus on the relationship between growth rate and phosphorus concentration and find that RNA allocation largely contributes to the commonly observed trend. This work emphasizes the potential role our model could play in connecting microorganisms to the surrounding environment while using realistic physiological representations.

Light-driven Proton Pumps as a Potential Regulator for Carbon Fixation in Marine Diatoms.

Diatoms are a major phytoplankton group responsible for approximately 20% of carbon fixation on Earth. They perform photosynthesis using light-harvesting chlo-rophylls located in plastids, an organelle obtained through eukaryote-eukaryote endosymbiosis. Microbial rhodopsin, a photoreceptor distinct from chlo-rophyll-based photosystems, was recently identified in some diatoms. However, the physiological function of diatom rhodopsin remains unclear. Heterologous expression techniques were herein used to investigate the protein function and subcellular localization of diatom rhodopsin. We demonstrated that diatom rhodopsin acts as a light-driven proton pump and localizes primarily to the outermost membrane of four membrane-bound complex plastids. Using model simulations, we also examined the effects of pH changes inside the plastid due to rhodopsin-mediated proton transport on photosynthesis. The results obtained suggested the involvement of rhodopsin-mediated local pH changes in a photosynthetic CO2-concentrating mechanism in rhodopsin-possessing diatoms.

The balance between photosynthesis and respiration explains the niche differentiation between Crocosphaera and Cyanothece.

Crocosphaera and Cyanothece are both unicellular, nitrogen-fixing cyanobacteria that prefer different environments. Whereas Crocosphaera mainly lives in nutrient-deplete, open oceans, Cyanothece is more common in coastal, nutrient-rich regions. Despite their physiological similarities, the factors separating their niches remain elusive. Here we performed physiological experiments on clone cultures and expand upon a simple ecological model to show that their different niches can be sufficiently explained by the observed differences in their photosynthetic capacities and rates of carbon (C) consumption. Our experiments revealed that Cyanothece has overall higher photosynthesis and respiration rates than Crocosphaera. A simple growth model of these microorganisms suggests that C storage and consumption are previously under-appreciated factors when evaluating the occupation of niches by different marine nitrogen fixers.

Modeling the elemental stoichiometry and silicon accumulation in diatoms.

Diatoms are important microorganisms involved in global primary production, nutrient cycling, and carbon sequestration. A unique feature of diatoms is their silica frustules, which impact sinking speed, defense against predators and viruses, and growth cycling. Thus, frustules are inherently linked to their role in ecosystems and biogeochemical cycles. However, constraints on cellular silicon levels remain unclear and few existing models resolve diatom elemental stoichiometry to specifically include variable silicon levels. Here, we use a coarse-grained model of the diatom, Thalassiosira pseudonana, compared with laboratory results to illustrate the relationship of silicon uptake with elemental stoichiometry of other nutrients. The model-data comparison suggests the balance between growth rate and silicon uptake constrains the amount of cellular silicon. Additionally, it expresses relationships between silicon, nitrogen, phosphorus, and carbon to changing growth rates in nitrogen-limited and phosphorus-limited regimes. First, our model-data comparison suggests Si uptake hits a maximum cellular quota at low growth rates and below this maximum there is independent Si uptake. In each nutrient regime, Si:N, Si:P, and Si:C decrease exponentially with growth rate when Si is below the maximum limit. This is explained by independent Si uptake and increased loss of Si to new cells. These results provide predictions of diatom stoichiometry and allocation, which can be used in ecosystem models to differentiate phytoplankton types to better represent diatoms' contribution to global biogeochemical cycles and ecosystems.

Saturating relationship between phytoplankton growth rate and nutrient concentration explained by macromolecular allocation.

Phytoplankton account for about a half of photosynthesis in the world, making them a key player in the ecological and biogeochemical systems. One of the key traits of phytoplankton is their growth rate because it indicates their productivity and affects their competitive capability. The saturating relationship between phytoplankton growth rate and environmental nutrient concentration has been widely observed yet the mechanisms behind the relationship remain elusive. Here we use a mechanistic model and metadata of phytoplankton to show that the saturating relationship between growth rate and nitrate concentration can be interpreted by intracellular macromolecular allocation. At low nitrate levels, the diffusive nitrate transport linearly increases with the nitrate concentration, while the internal nitrogen requirement increases with the growth rate, leading to a non-linear increase in the growth rate with nitrate. This increased nitrogen requirement is due to the increased allocation to biosynthetic and photosynthetic molecules. The allocation to these molecules reaches a maximum at high nitrate concentration and the growth rate ceases to increase despite high nitrate availability due to carbon limitation. The produced growth rate and nitrate relationships are consistent with the data of phytoplankton across taxa. Our study provides a macromolecular interpretation of the widely observed growth-nutrient relationship and highlights that the key control of the phytoplankton growth exists within the cell.

Low-Ammonium Environment Increases the Nutrient Exchange between Diatom-Diazotroph Association Cells and Facilitates Photosynthesis and N2 Fixation-a Mechanistic Modeling Analysis.

Diatom-diazotroph associations (DDAs) are one of the most important symbiotic dinitrogen (N2) fixing groups in the oligotrophic ocean. Despite their capability to fix N2, ammonium (NH4+) remains a key nitrogen (N) source for DDAs, and the effect of NH4+ on their metabolism remains elusive. Here, we developed a coarse-grained, cellular model of the DDA with NH4+ uptake and quantified how the level of extracellular NH4+ influences metabolism and nutrient exchange within the symbiosis. The model shows that, under a fixed growth rate, an increased NH4+ concentration may lower the required level of N2 fixation and photosynthesis, and decrease carbon (C) and N exchange. A low-NH4+ environment leads to more C and N in nutrient exchange and more fixed N2 to support a higher growth rate. With higher growth rates, nutrient exchange and metabolism increased. Our study shows a strong effect of NH4+ on metabolic processes within DDAs, and thus highlights the importance of in situ measurement of NH4+ concentrations.

Sinking Trichodesmium fixes nitrogen in the dark ocean.

The photosynthetic cyanobacterium Trichodesmium is widely distributed in the surface low latitude ocean where it contributes significantly to N2 fixation and primary productivity. Previous studies found nifH genes and intact Trichodesmium colonies in the sunlight-deprived meso- and bathypelagic layers of the ocean (200-4000 m depth). Yet, the ability of Trichodesmium to fix N2 in the dark ocean has not been explored. We performed 15N2 incubations in sediment traps at 170, 270 and 1000 m at two locations in the South Pacific. Sinking Trichodesmium colonies fixed N2 at similar rates than previously observed in the surface ocean (36-214 fmol N cell-1 d-1). This activity accounted for 40 ± 28% of the bulk N2 fixation rates measured in the traps, indicating that other diazotrophs were also active in the mesopelagic zone. Accordingly, cDNA nifH amplicon sequencing revealed that while Trichodesmium accounted for most of the expressed nifH genes in the traps, other diazotrophs such as Chlorobium and Deltaproteobacteria were also active. Laboratory experiments simulating mesopelagic conditions confirmed that increasing hydrostatic pressure and decreasing temperature reduced but did not completely inhibit N2 fixation in Trichodesmium. Finally, using a cell metabolism model we predict that Trichodesmium uses photosynthesis-derived stored carbon to sustain N2 fixation while sinking into the mesopelagic. We conclude that sinking Trichodesmium provides ammonium, dissolved organic matter and biomass to mesopelagic prokaryotes.

Crocosphaera as a Major Consumer of Fixed Nitrogen.

Crocosphaera watsonii (hereafter referred to as 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 picoeukaryotes. 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 picoeukaryotes and nondiazotrophic 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 heightening its potential significance in its ecosystem and in biogeochemical cycling. IMPORTANCE Crocosphaera watsonii is as a key nitrogen (N) supplier in marine ecosystems, and it has been estimated to contribute up to half of oceanic N2 fixation. Conversely, a recent study reported that Crocosphaera can assimilate combined N and proposed that unicellular diazotrophs can be competitors with non-N2 fixing phytoplankton for combined N. Despite its importance in nitrogen cycling, the methods by which Crocosphaera compete are not currently fully understood. Here, we present a new role of Crocosphaera as a combined-N consumer: a competitor against nondiazotrophic phytoplankton for combined N. In this study, we combined in situ microcosm experiments and an ecosystem model to quantitatively evaluate the combined-N consumption by Crocosphaera and other non-N2 fixing phytoplankton. Our 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.

Erratum to "Quantifying Cyanothece growth under DIC limitation" [Comput. Struct. Biotechnol. J. 19 (2021) 6456-6464].

[This corrects the article DOI: 10.1016/j.csbj.2021.11.036.].

Quantifying Cyanothece growth under DIC limitation.

The photoautotrophic, unicellular N2-fixer, Cyanothece, is a model organism that has been widely used to study photosynthesis regulation, the structure of photosystems, and the temporal segregation of carbon (C) and nitrogen (N) fixation in light and dark phases of the diel cycle. Here, we present a simple quantitative model and experimental data that together, suggest external dissolved inorganic carbon (DIC) concentration as a major limiting factor for Cyanothece growth, due to its high C-storage requirement. Using experimental data from a parallel laboratory study as a basis, we show that after the onset of the light period, DIC was rapidly consumed by photosynthesis, leading to a sharp drop in the rate of photosynthesis and C accumulation. In N2-fixing cultures, high rates of photosynthesis in the morning enabled rapid conversion of DIC to intracellular C storage, hastening DIC consumption to levels that limited further uptake. The N2-fixing condition allows only a small fraction of fixed C for cellular growth since a large fraction was reserved in storage to fuel night-time N2 fixation. Our model provides a framework for resolving DIC limitation in aquatic ecosystem simulations, where DIC as a growth-limiting factor has rarely been considered, and importantly emphasizes the effect of intracellular C allocation on growth rate that varies depending on the growth environment.

Modeled temperature dependencies of macromolecular allocation and elemental stoichiometry in phytoplankton.

Warming oceans may affect how phytoplankton allocate nutrients to essential cellular processes. Despite the potential impact of such processes on future biogeochemical cycles, questions remain about how temperature affects macromolecular allocation and elemental stoichiometry within phytoplankton cells. Here, we present a macromolecular model of phytoplankton and the effect of increasing temperature on the intracellular allocation of nutrients at a constant growth rate. When temperature increases under nitrogen (N) and phosphorus (P) co-limitation, the model shows less investment in phosphorus-rich RNA molecules relative to nitrogen-rich proteins, leading to a more severe decrease in cellular P:C than N:C causing increased cellular N:P values. Under P limitation, the model shows a similar pattern, but when excess P is available under N limitation, we predict lowered N:P due to the effect of luxury uptake of P. We reflected our model result on the surface ocean showing similar latitudinal patterns in N:P and P:C to observation and other model predictions, suggesting a considerable impact of temperature on constraining the elemental stoichiometry in the ocean.