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ABSTRACT 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. IMPORTANCE Trichodesmium 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. 

Abstract The proportion of major elements in marine organic matter links cellular processes to global nutrient, oxygen and carbon cycles. Differences in the C:N:P ratios of organic matter have been observed between ocean biomes, but these patterns have yet to be quantified from the underlying small-scale physiological and ecological processes. Here we use an ecosystem model that includes adaptive resource allocation within and between ecologically distinct plankton size classes to attribute the causes of global patterns in the C:N:P ratios. We find that patterns of N:C variation are largely driven by common physiological adjustment strategies across all phytoplankton, while patterns of N:P are driven by ecological selection for taxonomic groups with different phosphorus storage capacities. Although N:C varies widely due to cellular adjustment to light and nutrients, its latitudinal gradient is modest because of depth-dependent trade-offs between nutrient and light availability. Strong latitudinal variation in N:P reflects an ecological balance favouring small plankton with lower P storage capacity in the subtropics, and larger eukaryotes with a higher cellular P storage capacity in nutrient-rich high latitudes. A weaker N:P difference between southern and northern hemispheres, and between the Atlantic and Pacific oceans, reflects differences in phosphate available for cellular storage. Despite simulating only two phytoplankton size classes, the emergent global variability of elemental ratios resembles that of all measured species, suggesting that the range of growth conditions and ecological selection sustain the observed diversity of stoichiometry among phytoplankton. 

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. 

ABSTRACT The kinetics of microbial respiration suggest that, if excess organic matter is present, oxygen should fall to nanomolar levels, in the range of the Michaelis-Menten constants (Km). Yet even in many biologically productive coastal regions, lowest observed O2 concentrations often remain several orders of magnitude higher than respiratory Km values. We propose the Hypoxic Barrier Hypothesis (HBH) to explain this apparent discrepancy. The HBH postulates that oxidative enzymes involved in organic matter catabolism are kinetically limited by O2 at concentrations far higher than the thresholds for respiration. We found support for the HBH in a meta-analysis of 1137 O2 Km values reported in the literature: the median value for terminal respiratory oxidases was 350 nM, but for other oxidase types the median value was 67 μM. The HBH directs our attention to the kinetic properties of an important class of oxygen-dependent reactions that could help explain the trajectories of ocean ecosystems experiencing O2 stress. IMPORTANCE Declining ocean oxygen associated with global warming and climate change is impacting marine ecosystems across scales from microscopic planktonic communities to global fisheries. We report a fundamental dichotomy in the affinity of enzymes for oxygen. The importance of this observation has yet to be fully assessed, but it is predicted to impact the rate at which organic matter is oxidized in hypoxic ecosystems, and the types of organic matter that accumulate. Competition between intracellular enzymes for oxygen may also have impacted microbial strategies of adaptation to suboxia. 

Abstract. Global projections for ocean conditions in 2100 predict that the North Pacific will experience some of the largest changes. Coastal processes that drive variability in the region can alter these projected changes but are poorly resolved by global coarse-resolution models. We quantify the degree to which local processes modify biogeochemical changes in the eastern boundary California Current System (CCS) using multi-model regionally downscaled climate projections of multiple climate-associated stressors (temperature, O2, pH, saturation state (Ω), and CO2). The downscaled projections predict changes consistent with the directional change from the global projections for the same emissions scenario. However, the magnitude and spatial variability of projected changes are modified in the downscaled projections for carbon variables. Future changes in pCO2 and surface Ω are amplified, while changes in pH and upper 200 m Ω are dampened relative to the projected change in global models. Surface carbon variable changes are highly correlated to changes in dissolved inorganic carbon (DIC), pCO2 changes over the upper 200 m are correlated to total alkalinity (TA), and changes at the bottom are correlated to DIC and nutrient changes. The correlations in these latter two regions suggest that future changes in carbon variables are influenced by nutrient cycling, changes in benthic–pelagic coupling, and TA resolved by the downscaled projections. Within the CCS, differences in global and downscaled climate stressors are spatially variable, and the northern CCS experiences the most intense modification. These projected changes are consistent with the continued reduction in source water oxygen; increase in source water nutrients; and, combined with solubility-driven changes, altered future upwelled source waters in the CCS. The results presented here suggest that projections that resolve coastal processes are necessary for adequate representation of the magnitude of projected change in carbon stressors in the CCS.