A model of time-dependent macromolecular and elemental composition of phytoplankton.

Phytoplankton Chl:C:N:P ratios are important from both an ecological and a biogeochemical perspective. We show that these elemental ratios can be represented by a phytoplankton physiological model of low complexity that includes major cellular macromolecular pools. In particular, our model resolves time-dependent intracellular pools of chlorophyll, proteins, nucleic acids, carbohydrates/lipids, and N and P storage. Batch culture data for two diatom and two prasinophyte species are used to constrain parameters that represent specific allocation traits and strategies. A key novelty is the simultaneous estimation of physiological parameters for two phytoplankton groups of such different sizes. The number of free parameters is reduced by assuming (i) allometric scaling for maximum uptake rates, (ii) shared half-saturation constants for synthesis of functional macromolecules, (iii) shared exudation rates of functional macromolecules across the species. The rationale behind this assumption is that across the different species, the same or similar processes, enzymes, and metabolites play a role in key physiological processes. For the turnover numbers of macromolecular synthesis and storage exudation rates, differences between diatoms and prasinophytes need to be taken into account to obtain a good fit. Our model fits suggest that the parameters related to storage dynamics dominate the differences in the C:N:P ratios between the different phytoplankton groups. Since descriptions of storage dynamics are still incomplete and imprecise, predictions of C:N:P ratios by phytoplankton models likely have a large uncertainty.

Common environmental stress responses in a model marine diatom.

Marine planktonic diatoms are among the most important contributors to phytoplankton blooms and marine net primary production. Their ecological success has been attributed to their ability to rapidly respond to changing environmental conditions. Here, we report common molecular mechanisms used by the model marine diatom Thalassiosira pseudonana to respond to 10 diverse environmental stressors using RNA-Seq analysis. We identify a specific subset of 1076 genes that are differentially expressed in response to stressors that induce an imbalance between energy or resource supply and metabolic capacity, which we termed the diatom environmental stress response (d-ESR). The d-ESR is primarily composed of genes that maintain proteome homeostasis and primary metabolism. Photosynthesis is strongly regulated in response to environmental stressors but chloroplast-encoded genes were predominantly upregulated while the nuclear-encoded genes were mostly downregulated in response to low light and high temperature. In aggregate, these results provide insight into the molecular mechanisms used by diatoms to respond to a range of environmental perturbations and the unique role of the chloroplast in managing environmental stress in diatoms. This study facilitates our understanding of the molecular mechanisms underpinning the ecological success of diatoms in the ocean.

Elemental stoichiometry of the key calcifying marine phytoplankton Emiliania huxleyi under ocean climate change: A meta-analysis.

The elemental composition of marine microorganisms (their C:N:P ratio, or stoichiometry) is central to understanding the biotic and biogeochemical processes underlying key marine ecosystem functions. Phytoplankton C:N:P is species specific and flexible to changing environmental conditions. However, bulk or fixed phytoplankton stoichiometry is usually assumed in biogeochemical and ecological models because more realistic, environmentally responsive C:N:P ratios have yet to be defined for key functional groups. Here, a comprehensive meta-analysis of experimental laboratory data reveals the variable C:N:P stoichiometry of Emiliania huxleyi, a globally significant calcifying phytoplankton species. Mean C:N:P of E. huxleyi is 124C:16N:1P under control conditions (i.e. growth not limited by one or more environmental stressors) and shows a range of responses to changes in nutrient and light availability, temperature and pCO2 . Macronutrient limitation caused strong shifts in stoichiometry, increasing N:P and C:P under P deficiency (by 305% and 493% respectively) and doubling C:N under N deficiency. Responses to light, temperature and pCO2 were mixed but typically shifted cellular elemental content and C:N:P stoichiometry by ca. 30% or less. Besides these independent effects, the interactive effects of multiple environmental changes on E. huxleyi stoichiometry under future ocean conditions could be additive, synergistic or antagonistic. To synthesise our meta-analysis results, we explored how the cellular elemental content and C:N:P stoichiometry of E. huxleyi may respond to two hypothetical future ocean scenarios (increased temperature, irradiance and pCO2 combined with either N deficiency or P deficiency) if an additive effect is assumed. Both future scenarios indicate decreased calcification (which is predominantly sensitive to elevated pCO2 ), increased C:N, and up to fourfold shifts in C:P and N:P. Our results strongly suggest that climate change will significantly alter the role of E. huxleyi (and potentially other calcifying phytoplankton species) in marine biogeochemical processes.

Conservation and architecture of housekeeping genes in the model marine diatom Thalassiosira pseudonana.

Housekeeping genes (HKGs) are constitutively expressed with low variation across tissues/conditions. They are thought to be highly conserved and fundamental to cellular maintenance, with distinctive genomic features. Here, we identify 1505 HKGs in the unicellular marine diatom Thalassiosira pseudonana based on an RNA-seq analysis of 232 samples taken under 12 experimental conditions over 0-72 h. We identify promising internal reference genes (IRGs) for T. pseudonana from the most stably expressed HKGs. A comparative analysis indicates < 18% of HKGs in T. pseudonana have orthologs in other eukaryotes, including other diatom species. Contrary to work on human tissues, T. pseudonana HKGs are longer than non-HKGs, due to elongated introns. More ancient HKGs tend to be shorter than more recent HKGs, and expression levels of HKGs decrease more rapidly with gene length relative to non-HKGs. Our results indicate that HKGs are highly variable across the tree of life and thus unlikely to be universally fundamental for cellular maintenance. We hypothesize that the distinct genomic features of HKGs of T. pseudonana may be a consequence of selection pressures associated with high expression and low variance across conditions.

Anthropogenic climate change impacts on copepod trait biogeography.

Copepods are among the most abundant marine metazoans and form a key link between marine primary producers, higher trophic levels, and carbon sequestration pathways. Climate change is projected to change surface ocean temperature by up to 4°C in the North Atlantic with many associated changes including slowing of the overturning circulation, areas of regional freshening, and increased salinity and reductions in nutrients available in the euphotic zone over the next century. These changes will lead to a restructuring of phytoplankton and zooplankton communities with cascading effects throughout the food web. Here we employ observations of copepods, projected changes in ocean climate, and species distribution models to show how climate change may affect the distribution of copepod species in the North Atlantic. On average species move northeast at a rate of 14.1 km decade-1 . Species turnover in copepod communities will range from 5% to 75% with the highest turnover rates concentrated in regions of pronounced temperature increase and decrease. The changes in species range vary according to copepod traits with the largest effects found to occur in the cooling, freshening area in the subpolar North Atlantic south of Greenland and in an area of significant warming along the Scotian shelf. Large diapausing copepods (>2.5 mm) which are higher in lipids and a crucial food source for whales, may have an advantage in the cooling waters due to their life-history strategy that facilitates their survival in the arctic environment. Carnivorous copepods show a basin wide increase in species richness and show significant habitat area increases when their distribution moves poleward while herbivores see significant habitat area losses. The trait-specific effects highlight the complex consequences of climate change for the marine food web.

Dynamic Photophysiological Stress Response of a Model Diatom to Ten Environmental Stresses.

Stressful environmental conditions can induce many different acclimation mechanisms in marine phytoplankton, resulting in a range of changes in their photophysiology. Here we characterize the common photophysiological stress response of the model diatom Thalassiosira pseudonana to ten environmental stressors and identify diagnostic responses to particular stressors. We quantify the magnitude and temporal trajectory of physiological parameters including the functional absorption cross-section of PSII (σPSII ), quantum efficiency of PSII, non-photochemical quenching (NPQ), cell volume, Chl a, and carotenoid (Car) content in response to nutrient starvation (nitrogen (N), phosphorus (P), silicon (Si), and iron (Fe)), changes in temperature, irradiance, pH, and reactive oxygen species (ROS) over 5 time points (0, 2, 6, 24, 72 h). We find changes in conditions: temperature, irradiance, and ROS, often result in the most rapid changes in photophysiological parameters (<2 h), and in some cases are followed by recovery. In contrast, nutrient starvation (N, P, Si, Fe) often has slower (6-72 h) but ultimately larger magnitude effects on many photophysiological parameters. Diagnostic changes include large increases in cell volume under Si-starvation, very large increases in NPQ under P-starvation, and large decreases in the σPSII under high light. The ultimate goal of this analysis is to facilitate and enhance the interpretation of fluorescence data and our understanding of phytoplankton photophysiology from laboratory and field studies.

Photosynthetic adaptation to light availability shapes the ecological success of bloom-forming cyanobacterium Pseudanabaena to iron limitation.

The poorly understood filamentous cyanobacterium Pseudanabaena is commonly epiphytic on Microcystis colonies and their abundances are often highly correlated during blooms. The response and adaptation of Microcystis to iron limitation have been extensively studied, but the strategies Pseudanabaena uses to respond to iron limitation are largely unknown. Here, physiological responses to iron limitation were compared between one Pseudanabaena and two Microcystis strains grown under different light intensities. The results showed that low-intensity light exacerbated, but high-intensity light alleviated, the negative effect of iron limitation on Pseudanabaena growth relative to two Microcystis strains. It was found that robust light-harvesting and photosynthetic efficiency allowed adaptation of Pseudanabaena to low light availability relative to two Microcystis strains only during iron sufficiency. The results also indicated that a larger investment in the photosynthetic antenna probably contributed to light/iron co-limitation of Pseudanabaena relative to two Microcystis strains under both light and iron limitation. Furthermore, the lower antenna pigments/chlorophyll a ratio and photosynthetic efficiency, and higher nonphotochemical quenching and saturation irradiance provided Pseudanabaena photoadaptation and photoprotection advantages over the two Microcystis strains under the high-light condition. The lower investment in antenna pigments of Pseudanabaena than the two Microcystis strains under high-light intensity is likely an efficient strategy for both saving iron quotas and decreasing photosensitivity. Therefore, when compared with Microcystis, the high plasticity of antenna pigments, along with the excellent photoadaptation and photoprotection ability of Pseudanabaena, probably ensures its ecological success under iron limitation when light is sufficient.

The macromolecular composition of noncalcified marine macroalgae.

The macromolecular composition of macroalgae influences nutrient flow and food quality in aquatic ecosystems and the value of macroalgae species for human consumption, aquaculture, biofuels, and other applications. We used literature data (125 publications, 1,117 observations) and a hierarchal Bayesian statistical model to estimate the average macromolecular composition, protein, lipid, and carbohydrate of macroalgae as a whole and at the phylum level. Our focus was on marine, noncalcified macroalgae sampled from wild-grown populations in the field. We found that the median macromolecular composition is 9.98% protein, 2.7% lipid, 48.5% carbohydrate, and 31.8% ash as percent dry weight. We compared the median macromolecular content of macroalgae to microalgae and herbaceous plants and test for differences in macromolecular content across macroalgal phyla. Macroalgae were much more enriched in carbohydrate and minerals than the microalgae and lower in protein and lipid than many herbaceous plants. Rhodophyte macroalgae have significantly less lipid and more protein and the Ochrophyte macroalgae have significantly less protein than the average.

Anthropogenic climate change drives shift and shuffle in North Atlantic phytoplankton communities.

Anthropogenic climate change has shifted the biogeography and phenology of many terrestrial and marine species. Marine phytoplankton communities appear sensitive to climate change, yet understanding of how individual species may respond to anthropogenic climate change remains limited. Here, using historical environmental and phytoplankton observations, we characterize the realized ecological niches for 87 North Atlantic diatom and dinoflagellate taxa and project changes in species biogeography between mean historical (1951-2000) and future (2051-2100) ocean conditions. We find that the central positions of the core range of 74% of taxa shift poleward at a median rate of 12.9 km per decade (km⋅dec(-1)), and 90% of taxa shift eastward at a median rate of 42.7 km⋅dec(-1) The poleward shift is faster than previously reported for marine taxa, and the predominance of longitudinal shifts is driven by dynamic changes in multiple environmental drivers, rather than a strictly poleward, temperature-driven redistribution of ocean habitats. A century of climate change significantly shuffles community composition by a basin-wide median value of 16%, compared with seasonal variations of 46%. The North Atlantic phytoplankton community appears poised for marked shift and shuffle, which may have broad effects on food webs and biogeochemical cycles.

Physiological response of 10 phytoplankton species exposed to macondo oil and the dispersant, Corexit.

Culture experiments were conducted on ten phytoplankton species to examine their biological and physiological responses during exposure to oil and a combination of oil and dispersant. The species tested included a range of taxa typically found in the Gulf of Mexico such as cyanobacteria, chlorophytes, and diatoms. Cultures were exposed to Macondo surrogate oil using the water accommodated fraction (WAF), and dispersed oil using a chemically enhanced WAF (CEWAF) and diluted CEWAF, to replicate conditions following the Deepwater Horizon spill in the Gulf of Mexico. A range of responses were observed, that could broadly class the algae as either "robust" or "sensitive" to oil and/or dispersant exposure. Robust algae were identified as Synechococcus elongatus, Dunaliella tertiolecta, two pennate diatoms Phaeodactylum tricornutum and Navicula sp., and Skeletonema grethae CCMP775, and were largely unaffected by any of the treatments (no changes to growth rate or time spent in lag phase relative to controls). The rest of the phytoplankton, all centric diatoms, exhibited at least some combination of reduced growth rates or increased lag time in response to oil and/or dispersant exposure. Photophysiology did not have a strong treatment effect, with significant inhibition of photosynthetic efficiency (Fv /Fm ) only observed in the CEWAF, if at all. We found that the effects of oil and dispersants on phytoplankton physiology were species-dependent, and not always detrimental. This has significant implications on how oil spills might impact phytoplankton community structure and bloom dynamics in the Gulf of Mexico, which in turn impacts higher trophic levels.

Phytoplankton adapt to changing ocean environments.

Model projections indicate that climate change may dramatically restructure phytoplankton communities, with cascading consequences for marine food webs. It is currently not known whether evolutionary change is likely to be able to keep pace with the rate of climate change. For simplicity, and in the absence of evidence to the contrary, most model projections assume species have fixed environmental preferences and will not adapt to changing environmental conditions on the century scale. Using 15 y of observations from Station CARIACO (Carbon Retention in a Colored Ocean), we show that most of the dominant species from a marine phytoplankton community were able to adapt their realized niches to track average increases in water temperature and irradiance, but the majority of species exhibited a fixed niche for nitrate. We do not know the extent of this adaptive capacity, so we cannot conclude that phytoplankton will be able to adapt to the changes anticipated over the next century, but community ecosystem models can no longer assume that phytoplankton cannot adapt.

Marine extinction risk shaped by trait-environment interactions over 500 million years.

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait-based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta-analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait-based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life-habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow-ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3-3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.

The biogeography of marine plankton traits.

Changes in marine plankton communities driven by environmental variability impact the marine food web and global biogeochemical cycles of carbon and other elements. To predict and assess these community shifts and their consequences, ecologists are increasingly investigating how the functional traits of plankton determine their relative fitness along environmental and biological gradients. Laboratory, field and modelling studies are adopting this trait-based approach to map the biogeography of plankton traits that underlies variations in plankton communities. Here, we review progress towards understanding the regulatory roles of several key plankton functional traits, including cell size, N2 -fixation and mixotrophy among phytoplankton, and body size, ontogeny and feeding behaviour for zooplankton. The trait biogeographical approach sheds light on what structures plankton communities in the current ocean, as well as under climate change scenarios, and also allows for finer resolution of community function because community trait composition determines the rates of significant processes, including carbon export. Although understanding of trait biogeography is growing, uncertainties remain that stem, in part, from the paucity of observations describing plankton functional traits. Thus, in addition to recommending widespread adoption of the trait-based approach, we advocate for enhanced collection, standardisation and dissemination of plankton functional trait data.

Density regulation amplifies environmentally induced population fluctuations.

Background: Density-dependent regulation is ubiquitous in population dynamics, and its potential interaction with environmental stochasticity complicates the characterization of the random component of population dynamics. Yet, this issue has not received attention commensurate with its relevance for descriptive and predictive modeling of population dynamics. Here we use a Bayesian modeling approach to investigate the contribution of density regulation to population variability in stochastic environments. Methods: We analytically derive a formula linking the stationary variance of population abundance/density under Gompertz regulation in a stochastic environment with constant variance to the environmental variance and the strength of density feedback, to investigate whether and how density regulation affects the stationary variance. We examine through simulations whether the relationship between stationary variance and density regulation inferred analytically under the Gompertz model carries over to the Ricker model, widely used in population dynamics modeling. Results: The analytical decomposition of the stationary variance under stochastic Gompertz dynamics implies higher variability for strongly regulated populations. Simulation results demonstrate that the pattern of increasing population variability with increasing density feedback found under the Gompertz model holds for the Ricker model as well, and is expected to be a general phenomenon with stochastic population models. We also analytically established and empirically validated that the square of the autoregressive parameter of the Gompertz model in AR(1) form represents the proportion of stationary variance due to density dependence. Discussion: Our results suggest that neither environmental stochasticity nor density regulation can alone explain the patterns of population variability in stochastic environments, as these two components of temporal variation interact, with a tendency for density regulation to amplify the magnitude of environmentally induced population fluctuations. This finding has far-reaching implications for population viability. It implies that intense intra-specific resource competition increases the risk of environment-driven population collapse at high density, making opportune harvesting a sensible practice for improving the resistance of managed populations such as fish stocks to environmental perturbations. The separation of density-dependent and density-independent processes will help improve population dynamics modeling, while providing a basis for evaluating the relative importance of these two categories of processes that remains a topic of long-standing controversy among ecologists.

Genomic architecture constrains macromolecular allocation in dinoflagellates.

Dinoflagellate genomes have a unique architecture that may constrain their physiological and biochemical responsiveness to environmental stressors. Here we quantified how nitrogen (N) starvation influenced macromolecular allocation and C:N:P of three photosynthetic marine dinoflagellates, representing different taxonomic classes and genome sizes. Dinoflagellates respond to nitrogen starvation by decreasing cellular nitrogen, protein and RNA content, but unlike many other eukaryotic phytoplankton examined RNA:protein is invariant. Additionally, 2 of the 3 species exhibit increases in cellular phosphorus and very little change in cellular carbon with N-starvation. As a consequence, N starvation induces moderate increases in C:N, but extreme decreases in N:P and C:P, relative to diatoms. Dinoflagellate DNA content relative to total C, N and P is much higher than similar sized diatoms, but similar to very small photosynthetic picoeukaryotes such as Ostreococcus. In aggregate these results indicate the accumulation of phosphate stores may be an important strategy employed by dinoflagellates to meet P requirements associated with the maintenance and replication of their large genomes.

Basin-scale biogeography of marine phytoplankton reflects cellular-scale optimization of metabolism and physiology.

Extensive microdiversity within Prochlorococcus, the most abundant marine cyanobacterium, occurs at scales from a single droplet of seawater to ocean basins. To interpret the structuring role of variations in genetic potential, as well as metabolic and physiological acclimation, we developed a mechanistic constraint-based modeling framework that incorporates the full suite of genes, proteins, metabolic reactions, pigments, and biochemical compositions of 69 sequenced isolates spanning the Prochlorococcus pangenome. Optimizing each strain to the local, observed physical and chemical environment along an Atlantic Ocean transect, we predicted variations in strain-specific patterns of growth rate, metabolic configuration, and physiological state, defining subtle niche subspaces directly attributable to differences in their encoded metabolic potential. Predicted growth rates covaried with observed ecotype abundances, affirming their significance as a measure of fitness and inferring a nonlinear density dependence of mortality. Our study demonstrates the potential to interpret global-scale ecosystem organization in terms of cellular-scale processes.

Evolutionary inheritance of elemental stoichiometry in phytoplankton.

The elemental composition of phytoplankton is a fusion of the evolutionary history of the host and plastid, resulting in differences in genetic constraints and selection pressures associated with environmental conditions. The evolutionary inheritance hypothesis predicts similarities in elemental composition within related taxonomic lineages of phytoplankton. To test this hypothesis, we measured the elemental composition (C, N, P, S, K, Mg, Ca, Sr, Fe, Mn, Zn, Cu, Co, Cd and Mo) of 14 phytoplankton species and combined these with published data from 15 more species from both marine and freshwater environments grown under nutrient-replete conditions. The largest differences in the elemental profiles of the species distinguish between the prokaryotic Cyanophyta and primary endosymbiotic events that resulted in the green and red plastid lineages. Smaller differences in trace element stoichiometry within the red and green plastid lineages are consistent with changes in trace elemental stoichiometry owing to the processes associated with secondary endosymbioses and inheritance by descent with modification.

Contrasting transcriptomic responses of a microbial eukaryotic community to oil and dispersant.

Dispersants can aid dispersion and biodegradation of oil in seawater, but the wider ecotoxicological effects of oil and dispersant to the base of marine food webs is unclear. Here we apply a metatranscriptomic approach to identify molecular responses of a natural marine microbial eukaryotic community to oil and chemically dispersed oil. Oil exposure stimulated the upregulation of ketogenesis in the eukaryotic community, which may alleviate carbon- and energy-limitation and reduce oxidative stress. In contrast, a chemically dispersed oil treatment stimulated eukaryotic genes and pathways consistent with nitrogen and oxygen depletion. These results suggest that the addition of dispersant may elevate bacterial biodegradation of crude oil, indirectly increasing competition for nitrogen between prokaryotic and eukaryotic communities as oxygen consumption induces bacterial anaerobic respiration and denitrification. Eukaryotic microbial communities may mitigate some of the negative effects of oil exposure such as reduced photosynthesis and elevated oxidative stress, through ketosis, but the addition of dispersant to the oil fundamentally alters the environmental and ecological conditions and therefore the biochemical response of the eukaryotic community.

Cell size trade-offs govern light exploitation strategies in marine phytoplankton.

Marine phytoplankton show complex community structures and biogeographic distributions, the net results of physiological and ecological trade-offs of species responses to fluctuating, heterogeneous environments. We analysed photosynthesis, responses to variable light and macromolecular allocations across a size panel of marine centric diatoms. The diatoms have strong capacities to withstand and exploit fluctuating light, when compared with picophytoplankton. Within marine diatoms, small species show larger effective cross-sections for photochemistry, and fast metabolic repair of photosystem II after photoinactivation. In contrast, large diatoms show lower susceptibility to photoinactivation, and therefore incur lower costs to endure short-term exposures to high light, especially under conditions that limit metabolic rates. This size scaling of key photophysiological parameters thus helps explain the relative competitive advantages of larger versus smaller species under different environmental regimes, with implications for the function of the biogenic carbon pump. These results provide a mechanistic framework to explain and predict shifts in marine phytoplankton community size structure with changes in surface irradiance and mixed layer depth.