Environmental variability is an inherent feature of natural systems which complicates predictions of species interactions. Primarily, the complexity in predicting the response of organisms to environmental fluctuations is in part because species' responses to abiotic factors are non-linear, even in stable conditions. Temperature exerts a major control over phytoplankton growth and physiology, yet the influence of thermal fluctuations on growth and competition dynamics is largely unknown. To investigate the limits of coexistence in variable environments, stable mixed cultures with constant species abundance ratios of the marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana, were exposed to different temperature fluctuation regimes (n = 17) under high and low nitrogen (N) conditions. Here we demonstrate that phytoplankton exhibit substantial resilience to temperature variability. The time required to observe a shift in the species abundance ratio decreased with increasing fluctuations, but coexistence of the two model species under high N conditions was disrupted only when amplitudes of temperature fluctuation were high (+/- 8.2 degrees C). N limitation caused the thermal amplitude for disruption of species coexistence to become lower (+/- 5.9 degrees C). Furthermore, once stable conditions were reinstated, the two species differed in their ability to recover from temperature fluctuations. Our findings suggest that despite the expectation of unequal effect of fluctuations on different competitors, cycles in environmental conditions may reduce the rate of species replacement when amplitudes remain below a certain threshold. Beyond these thresholds, competitive exclusion could, however, be accelerated, suggesting that aquatic heatwaves and N availability status are likely to lead to abrupt and unpredictable restructuring of phytoplankton community composition.

Predicting spatiotemporal distributions of phytoplankton biomass and community composition heavily relies on experimental studies that document how environmental conditions influence population growth rates. In unicellular phytoplankton, the net population growth rate is the difference between the cell division rate and the death rate. Along with predation and disease, phytoplankton mortality arises from abiotic stress. Although the effect of temperature on the net population growth rate is well understood, studies examining thermally induced death rates in phytoplankton are scarce. We investigated how cell division and death rates of the diatom Phaeodactylum tricornutum varied within its thermal tolerance limits (thermal niche), and at temperatures just above its upper thermal tolerance limit. We show that death rates were largely independent of temperature when P. tricornutum was grown within its thermal niche, but increased significantly at temperatures that approached or exceeded its upper thermal tolerance limit. Furthermore, the sensitivity of mortality increased with the duration of exposure to heat stress and was affected by the pre-acclimation temperature. Heat waves can be expected to significantly affect phytoplankton mortality episodically. The increasing frequency of heat waves accompanying global warming can be expected to drive changes in phytoplankton community structure due to interspecific variability of thermal niches with potential implications for food web dynamics and biogeochemical cycles.

Estimates of marine N2 fixation range from 52 to 73 Tg N/year, of which we calculate up to 84% is from Trichodesmium based on previous measurements of nifH gene abundance and our new model of Trichodesmium growth. Here, we assess the likely effects of four major climate change‐related abiotic factors on the spatiotemporal distribution and growth potential of Trichodesmium for the last glacial maximum (LGM), the present (2006–2015) and the end of this century (2100) by mapping our model of Trichodesmium growth onto inferred global surface ocean fields of pCO2, temperature, light and Fe. We conclude that growth rate was severely limited by low pCO2 at the LGM, that current pCO2 levels do not significantly limit Trichodesmium growth and thus, the potential for enhanced growth from future increases in CO2 is small. We also found that the area of the ocean where sea surface temperatures (SST) are within Trichodesmium's thermal niche increased by 32% from the LGM to present, but further increases in SST due to continued global warming will reduce this area by 9%. However, the range reduction at the equator is likely to be offset by enhanced growth associated with expansion of regions with optimal or near optimal Fe and light availability. Between now and 2100, the ocean area of optimal SST and irradiance is projected to increase by 7%, and the ocean area of optimal SST, irradiance and iron is projected to increase by 173%. Given the major contribution of this keystone species to annual N2 fixation and thus pelagic ecology, biogeochemistry and CO2 sequestration, the projected increase in the geographical range for optimal growth could provide a negative feedback to increasing atmospheric CO2 concentrations.

Abstract The distribution of marine phytoplankton will shift alongside changes in marine environments, leading to altered species frequencies and community composition. An understanding of the response of mixed populations to abiotic changes is required to adequately predict how environmental change may affect the future composition of phytoplankton communities. This study investigated the growth and competitive ability of two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana, along a temperature gradient (9–35°C) spanning the thermal niches of both species under both high‐nitrogen nutrient‐replete and low‐nitrogen nutrient‐limited conditions. Across this temperature gradient, the competitive outcome under both nutrient conditions at any assay temperature, and the critical temperature at which competitive advantage shifted from one species to the other, was well predicted by the temperature dependencies of the growth rates of the two species measured in monocultures. The temperature at which the competitive advantage switched from P. tricornutum to T. pseudonana increased from 18.8°C under replete conditions to 25.3°C under nutrient‐limited conditions. Thus, P. tricornutum was a better competitor over a wider temperature range in a low N environment. Being able to determine the competitive outcomes from physiological responses of single species to environmental changes has the potential to significantly improve the predictive power of phytoplankton spatial distribution and community composition models.

Photosystem II (PSII) photochemistry is the ultimate source of reducing power for phytoplankton primary productivity (PhytoPP). Single turnover active chlorophyll fluorometry (STAF) provides a non-intrusive method that has the potential to measure PhytoPP on much wider spatiotemporal scales than is possible with more direct methods such as 14 C fixation and O 2 evolved through water oxidation. Application of a STAF-derived absorption coefficient for PSII light-harvesting (a LHII ) provides a method for estimating PSII photochemical flux on a unit volume basis (JV PII ). Within this study, we assess potential errors in the calculation of JV PII arising from sources other than photochemically active PSII complexes (baseline fluorescence) and the package effect. Although our data show that such errors can be significant, we identify fluorescence-based correction procedures that can be used to minimize their impact. For baseline fluorescence, the correction incorporates an assumed consensus PSII photochemical efficiency for dark-adapted material. The error generated by the package effect can be minimized through the ratio of variable fluorescence measured within narrow wavebands centered at 730 nm, where the re-absorption of PSII fluorescence emission is minimal, and at 680 nm, where re-absorption of PSII fluorescence emission is maximal. We conclude that, with incorporation of these corrective steps, STAF can provide a reliable estimate of JV PII and, if used in conjunction with simultaneous satellite measurements of ocean color, could take us significantly closer to achieving the objective of obtaining reliable autonomous estimates of PhytoPP.

As atmospheric CO2 concentrations increase, so too does the dissolved CO2 and HCO3- concentrations in the world's oceans. There are still many uncertainties regarding the biological response of key groups of organisms to these changing conditions, which is crucial for predicting future species distributions, primary productivity rates, and biogeochemical cycling. In this study, we established the relationship between gross photosynthetic O2 evolution and light-dependent O2 consumption in Trichodesmium erythraeum IMS101 acclimated to three targeted pCO2 concentrations (180 µmol mol-1=low-CO2, 380 µmol mol-1=mid-CO2, and 720 µmol mol-1=high-CO2). We found that biomass- (carbon) specific, light-saturated maximum net O2 evolution rates (PnC,max) and acclimated growth rates increased from low- to mid-CO2, but did not differ significantly between mid- and high-CO2. Dark respiration rates were five times higher than required to maintain cellular metabolism, suggesting that respiration provides a substantial proportion of the ATP and reductant for N2 fixation. Oxygen uptake increased linearly with gross O2 evolution across light intensities ranging from darkness to 1100 µmol photons m-2 s-1. The slope of this relationship decreased with increasing CO2, which we attribute to the increased energetic cost of operating the carbon-concentrating mechanism at lower CO2 concentrations. Our results indicate that net photosynthesis and growth of T. erythraeum IMS101 would have been severely CO2 limited at the last glacial maximum, but that the direct effect of future increases of CO2 may only cause marginal increases in growth.

Predictions of the ocean‐atmosphere flux of dimethyl sulfide will be improved by understanding what controls seasonal and regional variations in dimethylsulfoniopropionate (DMSP) production. To investigate the influence of high levels of irradiance including ultraviolet radiation (UVR), on DMSP synthesis rates ( μ DMSP) and inorganic carbon fixation ( μ POC) by natural phytoplankton communities, nine experiments were carried out at different locations in the low nutrient, high light environment of the northeastern Tropical Atlantic. Rates of μ DMSP and μ POC were determined by measuring the incorporation of inorganic 13 C into DMSP and particulate organic carbon. Based on measurements over discrete time intervals during the day, a unique μ DMSP vs. irradiance (P vs. E) relationship was established. Comparison is made with the P vs. E relationship for μ POC, indicating that light saturation of μ DMSP occurs at similar irradiance to μ POC and is closely coupled to carbon fixation on a diel basis. Photoinhibition during the middle of the day was exacerbated by exposure to UVR, causing an additional 55–60% inhibition of both μ DMSP and μ POC at the highest light levels. In addition, decreased production of DMSP in response to UVR‐induced photoxidative stress, contrasted with the increased net synthesis of photoprotective xanthophyll pigments. Together these results indicate that DMSP production by phytoplankton in the tropical ocean is not regulated in the short term by the necessity to control increasing photooxidative stress as irradiance increases during the day. The study provides new insight into the regulation of resource allocation into this biogeochemically important, multi‐functional compatible solute.

Trichodesmium plays a significant role in the oligotrophic oceans, fixing nitrogen in an area corresponding to half of the Earth's surface, representing up to 50% of new production in some oligotrophic tropical and subtropical oceans. Whilst Trichodesmium blooms at the surface exhibit a strong dependence on diazotrophy, colonies at depth or at the surface after a mixing event could be utilising additional N-sources. We conducted experiments to establish how acclimation to varying N-sources affects the growth, elemental composition, light absorption coefficient, N2 fixation, PSII electron transport rate and the relationship between net and gross photosynthetic O2 exchange in T. erythraeum IMS101. To do this, cultures were acclimated to growth medium containing NH4+ and NO3- (replete concentrations) or N2 only (diazotrophic control). The light dependencies of O2 evolution and O2 uptake were measured using membrane inlet mass spectrometry (MIMS), while PSII electron transport rates were measured from fluorescence light curves (FLCs). We found that at a saturating light intensity, Trichodesmium growth was ~ 10% and 13% lower when grown on N2 than with NH4+ and NO3-, respectively. Oxygen uptake increased linearly with net photosynthesis across all light intensities ranging from darkness to 1100 μmol photons m-2 s-1. The maximum rates and initial slopes of light response curves for C-specific gross and net photosynthesis and the slope of the relationship between gross and net photosynthesis increased significantly under non-diazotrophic conditions. We attribute these observations to a reduced expenditure of reductant and ATP for nitrogenase activity under non-diazotrophic conditions which allows NADPH and ATP to be re-directed to CO2 fixation and/or biosynthesis. The energy and reductant conserved through utilising additional N-sources could enhance Trichodesmium's productivity and growth and have major implications for its role in ocean C and N cycles.

Photosynthetic rates in the cyanobacterium Trichodesmium erythraeum appear to be a function of CO2, although numerical simulations of the carbon-concentrating mechanism show carboxylation to be mediated as a function of pH and HCO3–.

We have assessed how varying CO2 (180, 380, and 720 μatm) and growth light intensity (40 and 400 μmol photons m−2 s−1) affected Trichodesmium erythraeum IMS101 growth and photophysiology over free iron (Fe′) concentrations between 20 and 9,600 pM. We found significant iron dependencies of growth rate and the initial slope and maximal relative PSII electron transport rates (rPm). Under iron-limiting concentrations, high-light increased growth rates and rPm; possibly indicating a lower allocation of resources to iron-containing photosynthetic proteins. Higher CO2 increased growth rates across all iron concentrations, enabled growth to occur at lower Fe′ concentrations, increased rPm and lowered the iron half saturation constants for growth (Km). We attribute these CO2 responses to the operation of the CCM and the ATP spent/saved for CO2 uptake and transport at low and high CO2, respectively. It seems reasonable to conclude that T. erythraeum IMS101 can exhibit a high degree of phenotypic plasticity in response to CO2, light intensity and iron-limitation. These results are important given predictions of increased dissolved CO2 and water column stratification (i.e., higher light exposures) over the coming decades.

Trichodesmium is a globally important marine diazotroph that accounts for approximately 60 - 80% of marine biological N2 fixation and as such plays a key role in marine N and C cycles. We undertook a comprehensive assessment of how the growth rate of Trichodesmium erythraeum IMS101 was directly affected by the combined interactions of temperature, pCO2 and light intensity. Our key findings were: low pCO2 affected the lower temperature tolerance limit (Tmin) but had no effect on the optimum temperature (Topt) at which growth was maximal or the maximum temperature tolerance limit (Tmax); low pCO2 had a greater effect on the thermal niche width than low-light; the effect of pCO2 on growth rate was more pronounced at suboptimal temperatures than at supraoptimal temperatures; temperature and light had a stronger effect on the photosynthetic efficiency (Fv/Fm) than did CO2; and at Topt, the maximum growth rate increased with increasing CO2, but the initial slope of the growth-irradiance curve was not affected by CO2. In the context of environmental change, our results suggest that the (i) nutrient replete growth rate of Trichodesmium IMS101 would have been severely limited by low pCO2 at the last glacial maximum (LGM), (ii) future increases in pCO2 will increase growth rates in areas where temperature ranges between Tmin to Topt, but will have negligible effect at temperatures between Topt and Tmax, (iii) areal increase of warm surface waters (> 18°C) has allowed the geographic range to increase significantly from the LGM to present and that the range will continue to expand to higher latitudes with continued warming, but (iv) continued global warming may exclude Trichodesmium spp. from some tropical regions by 2100 where temperature exceeds Topt.

The equations used to account for the temperature dependence of biological processes, including growth and metabolic rates, are the foundations of our predictions of how global biogeochemistry and biogeography change in response to global climate change. We review and test the use of 12 equations used to model the temperature dependence of biological processes across the full range of their temperature response, including supra- and suboptimal temperatures. We focus on fitting these equations to thermal response curves for phytoplankton growth but also tested the equations on a variety of traits across a wide diversity of organisms. We found that many of the surveyed equations have comparable abilities to fit data and equally high requirements for data quality (number of test temperatures and range of response captured) but lead to different estimates of cardinal temperatures and of the biological rates at these temperatures. When these rate estimates are used for biogeographic predictions, differences between the estimates of even the best-fitting models can exceed the global biological change predicted for a decade of global warming. As a result, studies of the biological response to global changes in temperature must make careful consideration of model selection and of the quality of the data used for parametrizing these models.

Global ocean biogeochemistry models currently employed in climate change projections use highly simplified representations of pelagic food webs. These food webs do not necessarily include critical pathways by which ecosystems interact with ocean biogeochemistry and climate. Here we present a global biogeochemical model which incorporates ecosystem dynamics based on the representation of ten plankton functional types (PFTs): six types of phytoplankton, three types of zooplankton, and heterotrophic procaryotes. We improved the representation of zooplankton dynamics in our model through (a) the explicit inclusion of large, slow-growing macrozooplankton (e.g. krill), and (b) the introduction of trophic cascades among the three zooplankton types. We use the model to quantitatively assess the relative roles of iron vs. grazing in determining phytoplankton biomass in the Southern Ocean high-nutrient low-chlorophyll (HNLC) region during summer. When model simulations do not include macrozooplankton grazing explicitly, they systematically overestimate Southern Ocean chlorophyll biomass during the summer, even when there is no iron deposition from dust. When model simulations include a slow-growing macrozooplankton and trophic cascades among three zooplankton types, the high-chlorophyll summer bias in the Southern Ocean HNLC region largely disappears. Our model results suggest that the observed low phytoplankton biomass in the Southern Ocean during summer is primarily explained by the dynamics of the Southern Ocean zooplankton community, despite iron limitation of phytoplankton community growth rates. This result has implications for the representation of global biogeochemical cycles in models as zooplankton faecal pellets sink rapidly and partly control the carbon export to the intermediate and deep ocean.

SummaryLimitation of marine primary production by the availability of nitrogen or phosphorus is common. Emiliania huxleyi, a ubiquitous phytoplankter that plays key roles in primary production, calcium carbonate precipitation and production of dimethyl sulfide, often blooms in mid‐latitude at the beginning of summer when inorganic nutrient concentrations are low. To understand physiological mechanisms that allow such blooms, we examined how the proteome of E. huxleyi (strain 1516) responds to N and P limitation. We observed modest changes in much of the proteome despite large physiological changes (e.g. cellular biomass, C, N and P) associated with nutrient limitation of growth rate. Acclimation to nutrient limitation did however involve significant increases in the abundance of transporters for ammonium and nitrate under N limitation and for phosphate under P limitation. More notable were large increases in proteins involved in the acquisition of organic forms of N and P, including urea and amino acid/polyamine transporters and numerous C‐N hydrolases under N limitation and a large upregulation of alkaline phosphatase under P limitation. This highly targeted reorganization of the proteome towards scavenging organic forms of macronutrients gives unique insight into the molecular mechanisms that underpin how E. huxleyi has found its niche to bloom in surface waters depleted of inorganic nutrients.

Trichodesmium is a biogeochemically important marine cyanobacterium, responsible for a significant proportion of the annual 'new' nitrogen introduced into the global ocean. These non-heterocystous filamentous diazotrophs employ a potentially unique strategy of near-concurrent nitrogen fixation and oxygenic photosynthesis, potentially burdening Trichodesmium with a particularly high iron requirement due to the iron-binding proteins involved in these processes. Iron availability may therefore have a significant influence on the biogeography of Trichodesmium. Previous investigations of molecular responses to iron stress in this keystone marine microbe have largely been targeted. Here a holistic approach was taken using a label-free quantitative proteomics technique (MSE) to reveal a sophisticated multi-faceted proteomic response of Trichodesmium erythraeum IMS101 to iron stress. Increased abundances of proteins known to be involved in acclimation to iron stress and proteins known or predicted to be involved in iron uptake were observed, alongside decreases in the abundances of iron-binding proteins involved in photosynthesis and nitrogen fixation. Preferential loss of proteins with a high iron content contributed to overall reductions of 55-60% in estimated proteomic iron requirements. Changes in the abundances of iron-binding proteins also suggested the potential importance of alternate photosynthetic pathways as Trichodesmium reallocates the limiting resource under iron stress. Trichodesmium therefore displays a significant and integrated proteomic response to iron availability that likely contributes to the ecological success of this species in the ocean.

The advent of genomic-, transcriptomic- and proteomic-based approaches has revolutionized our ability to describe marine microbial communities, including biogeography, metabolic potential and diversity, mechanisms of adaptation, and phylogeny and evolutionary history. New interdisciplinary approaches are needed to move from this descriptive level to improved quantitative, process-level understanding of the roles of marine microbes in biogeochemical cycles and of the impact of environmental change on the marine microbial ecosystem. Linking studies at levels from the genome to the organism, to ecological strategies and organism and ecosystem response, requires new modelling approaches. Key to this will be a fundamental shift in modelling scale that represents micro-organisms from the level of their macromolecular components. This will enable contact with omics data sets and allow acclimation and adaptive response at the phenotype level (i.e. traits) to be simulated as a combination of fitness maximization and evolutionary constraints. This way forward will build on ecological approaches that identify key organism traits and systems biology approaches that integrate traditional physiological measurements with new insights from omics. It will rely on developing an improved understanding of ecophysiology to understand quantitatively environmental controls on microbial growth strategies. It will also incorporate results from experimental evolution studies in the representation of adaptation. The resulting ecosystem-level models can then evaluate our level of understanding of controls on ecosystem structure and function, highlight major gaps in understanding and help prioritize areas for future research programs. Ultimately, this grand synthesis should improve predictive capability of the ecosystem response to multiple environmental drivers.