Physiological and morphological plasticity in response to nitrogen availability of a yeast widely distributed in the open ocean.

Yeasts are prevalent in the open ocean, yet we have limited understanding of their ecophysiological adaptations, including their response to nitrogen availability, which can have a major role in determining the ecological potential of other planktonic microbes. In this study, we characterized the nitrogen uptake capabilities and growth responses of marine-occurring yeasts. Yeast isolates from the North Atlantic Ocean were screened for growth on diverse nitrogen substrates, and across a concentration gradient of three environmentally relevant nitrogen substrates: nitrate, ammonium, and urea. Three strains grew with enriched nitrate while two did not, demonstrating that nitrate utilization is present but not universal in marine yeasts, consistent with existing knowledge of nonmarine yeast strains. Naganishia diffluens MBA_F0213 modified the key functional trait of cell size in response to nitrogen concentration, suggesting yeast cell morphology changes along chemical gradients in the marine environment. Meta-analysis of the reference DNA barcode in public databases revealed that the genus Naganishia has a global ocean distribution, strengthening the environmental applicability of the culture-based observations. This study provides novel quantitative understanding of the ecophysiological and morphological responses of marine-derived yeasts to variable nitrogen availability in vitro, providing insight into the functional ecology of yeasts within pelagic open ocean environments.

Rapid evolution allows coexistence of highly divergent lineages within the same niche.

Marine microbial communities are extremely complex and diverse. The number of locally coexisting species often vastly exceeds the number of identifiable niches, and taxonomic composition often appears decoupled from local environmental conditions. This is contrary to the view that environmental conditions should select for a few locally well-adapted species. Here we use an individual-based eco-evolutionary model to show that virtually unlimited taxonomic diversity can be supported in highly evolving assemblages, even in the absence of niche separation. With a steady stream of heritable changes to phenotype, competitive exclusion may be weakened, allowing sustained coexistence of nearly neutral phenotypes with highly divergent lineages. This behaviour is robust even to abrupt environmental perturbations that might be expected to cause strong selection pressure and an associated loss of diversity. We, therefore, suggest that rapid evolution and individual-level variability are key drivers of species coexistence and maintenance of microbial biodiversity.

Environmental control of marine phytoplankton stoichiometry in the North Atlantic Ocean.

The stoichiometric coupling of carbon to limiting nutrients in marine phytoplankton regulates the magnitude of biological carbon sequestration in the ocean. While clear links between plankton C:N ratios and environmental drivers have been identified, the nature and direction of these links, as well as their underlying physiological and ecological controls, remain uncertain. We show, with a well-constrained mechanistic model of plankton ecophysiology, that while nitrogen availability and temperature emerge as the main drivers of phytoplankton C:N stoichiometry in the North Atlantic, the biological mechanisms involved vary depending on the spatiotemporal scale and region considered. We find that phytoplankton C:N stoichiometry is overall controlled by nitrogen availability below 40° N, predominantly driven by ecoevolutionary shifts in the functional composition of the phytoplankton communities, while phytoplankton stoichiometric plasticity in response to dropping temperatures and increased grazing pressure dominates at higher latitudes. Our findings highlight the potential of "organisms-to-ecosystems" modeling approaches based on mechanistic models of plankton biology accounting for physiology, ecology, and trait evolution to explore and explain complex observational data and ultimately improve the predictions of global ocean models.

Selective constraints on global plankton dispersal.

Marine microbial communities are highly interconnected assemblages of organisms shaped by ecological drift, natural selection, and dispersal. The relative strength of these forces determines how ecosystems respond to environmental gradients, how much diversity is resident in a community or population at any given time, and how populations reorganize and evolve in response to environmental perturbations. In this study, we introduce a globally resolved population-genetic ocean model in order to examine the interplay of dispersal, selection, and adaptive evolution and their effects on community assembly and global biogeography. We find that environmental selection places strong constraints on global dispersal, even in the face of extremely high assumed rates of adaptation. Changing the relative strengths of dispersal, selection, and adaptation has pronounced effects on community assembly in the model and suggests that barriers to dispersal play a key role in the structuring of marine communities, enhancing global biodiversity and the importance of local historical contingencies.

Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness.

The end-Cretaceous bolide impact triggered the devastation of marine ecosystems. However, the specific kill mechanism(s) are still debated, and how primary production subsequently recovered remains elusive. We used marine plankton microfossils and eco-evolutionary modeling to determine strategies for survival and recovery, finding that widespread phagotrophy (prey ingestion) was fundamental to plankton surviving the impact and also for the subsequent reestablishment of primary production. Ecological selectivity points to extreme post-impact light inhibition as the principal kill mechanism, with the marine food chain temporarily reset to a bacteria-dominated state. Subsequently, in a sunlit ocean inhabited by only rare survivor grazers but abundant small prey, it was mixotrophic nutrition (autotrophy and heterotrophy) and increasing cell sizes that enabled the eventual reestablishment of marine food webs some 2 million years later.

The impact of marine nutrient abundance on early eukaryotic ecosystems.

The rise of eukaryotes to ecological prominence represents one of the most dramatic shifts in the history of Earth's biosphere. However, there is an enigmatic temporal lag between the emergence of eukaryotic organisms in the fossil record and their much later ecological expansion. In parallel, there is evidence for a secular increase in the availability of the key macronutrient phosphorus (P) in Earth's oceans. Here, we use an Earth system model equipped with a size-structured marine ecosystem to explore relationships between plankton size, trophic complexity, and the availability of marine nutrients. We find a strong dependence of planktonic ecosystem structure on ocean nutrient abundance, with a larger ocean nutrient inventory leading to greater overall biomass, broader size spectra, and increasing abundance of large Zooplankton. If existing estimates of Proterozoic marine nutrient levels are correct, our results suggest that increases in the ecological impact of eukaryotic algae and trophic complexity in eukaryotic ecosystems were directly linked to restructuring of the global P cycle associated with the protracted rise of surface oxygen levels. Our results thus suggest an indirect but potentially important mechanism by which ocean oxygenation may have acted to shape marine ecological function during late Proterozoic time.

The Size Dependence of Phytoplankton Growth Rates: A Trade-Off between Nutrient Uptake and Metabolism.

Rates of metabolism and population growth are often assumed to decrease universally with increasing organism size. Recent observations have shown, however, that maximum population growth rates among phytoplankton smaller than ∼6 µm in diameter tend to increase with organism size. Here we bring together observations and theory to demonstrate that the observed change in slope is attributable to a trade-off between nutrient uptake and the potential rate of internal metabolism. Specifically, we apply an established model of phytoplankton growth to explore a trade-off between the ability of cells to replenish their internal quota (which increases with size) and their ability to synthesize new biomass (which decreases with size). Contrary to the metabolic theory of ecology, these results demonstrate that rates of resource acquisition (rather than metabolism) provide the primary physiological constraint on the growth rates of some of the smallest and most numerically abundant photosynthetic organisms on Earth.

Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux.

Mixotrophic plankton, which combine the uptake of inorganic resources and the ingestion of living prey, are ubiquitous in marine ecosystems, but their integrated biogeochemical impacts remain unclear. We address this issue by removing the strict distinction between phytoplankton and zooplankton from a global model of the marine plankton food web. This simplification allows the emergence of a realistic trophic network with increased fidelity to empirical estimates of plankton community structure and elemental stoichiometry, relative to a system in which autotrophy and heterotrophy are mutually exclusive. Mixotrophy enhances the transfer of biomass to larger sizes classes further up the food chain, leading to an approximately threefold increase in global mean organism size and an ∼35% increase in sinking carbon flux.

Temperature-Correlated Changes in Phytoplankton Community Structure Are Restricted to Polar Waters.

Globally distributed observations of size-fractionated chlorophyll a and temperature were used to incorporate temperature dependence into an existing semi-empirical model of phytoplankton community size structure. The additional temperature-dependent term significantly increased the model's ability to both reproduce and predict observations of chlorophyll a size-fractionation at temperatures below 2°C. The most notable improvements were in the smallest (picoplankton) size-class, for which overall model fit was more than doubled, and predictive skill was increased by approximately 40%. The model was subsequently applied to generate global maps for three phytoplankton size classes, on the basis of satellite-derived estimates of surface chlorophyll a and sea surface temperature. Polar waters were associated with marked decline in the chlorophyll a biomass of the smallest cells, relative to lower latitude waters of equivalent total chlorophyll a. In the same regions a complementary increase was seen in the chlorophyll a biomass of larger size classes. These findings suggest that a warming and stratifying ocean will see a poleward expansion of the habitat range of the smallest phytoplankton, with the possible displacement of some larger groups that currently dominate. There was no evidence of a strong temperature dependence in tropical or sub-tropical regions, suggesting that future direct temperature effects on community structure at lower latitudes may be small.

When everything is not everywhere but species evolve: an alternative method to model adaptive properties of marine ecosystems.

The functional and taxonomic biogeography of marine microbial systems reflects the current state of an evolving system. Current models of marine microbial systems and biogeochemical cycles do not reflect this fundamental organizing principle. Here, we investigate the evolutionary adaptive potential of marine microbial systems under environmental change and introduce explicit Darwinian adaptation into an ocean modelling framework, simulating evolving phytoplankton communities in space and time. To this end, we adopt tools from adaptive dynamics theory, evaluating the fitness of invading mutants over annual timescales, replacing the resident if a fitter mutant arises. Using the evolutionary framework, we examine how community assembly, specifically the emergence of phytoplankton cell size diversity, reflects the combined effects of bottom-up and top-down controls. When compared with a species-selection approach, based on the paradigm that "Everything is everywhere, but the environment selects", we show that (i) the selected optimal trait values are similar; (ii) the patterns emerging from the adaptive model are more robust, but (iii) the two methods lead to different predictions in terms of emergent diversity. We demonstrate that explicitly evolutionary approaches to modelling marine microbial populations and functionality are feasible and practical in time-varying, space-resolving settings and provide a new tool for exploring evolutionary interactions on a range of timescales in the ocean.

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.

Biophysical aspects of resource acquisition and competition in algal mixotrophs.

Mixotrophic organisms combine autotrophic and heterotrophic nutrition and are abundant in both freshwater and marine environments. Recent observations indicate that mixotrophs constitute a large fraction of the biomass, bacterivory, and primary production in oligotrophic environments. While mixotrophy allows greater flexibility in terms of resource acquisition, any advantage must be traded off against an associated increase in metabolic costs, which appear to make mixotrophs uncompetitive relative to obligate autotrophs and heterotrophs. Using an idealized model of cell physiology and community competition, we identify one mechanism by which mixotrophs can effectively outcompete specialists for nutrient elements. At low resource concentrations, when the uptake of nutrients is limited by diffusion toward the cell, the investment in cell membrane transporters can be minimized. In this situation, mixotrophs can acquire limiting elements in both organic and inorganic forms, outcompeting their specialist competitors that can utilize only one of these forms. This advantage can be enough to offset as much as a twofold increase in additional metabolic costs incurred by mixotrophs. This mechanism is particularly relevant for the maintenance of mixotrophic populations and productivity in the highly oligotrophic subtropical oceans.