Projected expansion of Trichodesmium's geographical distribution and increase in growth potential in response to climate change.

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.

CO2 modulation of the rates of photosynthesis and light-dependent O2 consumption in Trichodesmium.

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.

An Integrated Response of Trichodesmium erythraeum IMS101 Growth and Photo-Physiology to Iron, CO2, and Light Intensity.

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.

The physiological cost of diazotrophy for Trichodesmium erythraeum IMS101.

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.

Inorganic carbon and pH dependency of photosynthetic rates in Trichodesmium.

Increasing atmospheric CO2 concentrations are leading to increases in dissolved CO2 and HCO3- concentrations and decreases in pH and CO32- in the world's oceans. There remain many uncertainties as to the magnitude of biological responses of key organisms to these chemical changes. In this study, we established the relationship between photosynthetic carbon fixation rates and pH, CO2, and HCO3- concentrations in the diazotroph, Trichodesmium erythraeum IMS101. Inorganic 14C-assimilation was measured in TRIS-buffered artificial seawater medium where the absolute and relative concentrations of CO2, pH, and HCO3- were manipulated. First, we varied the total dissolved inorganic carbon concentration (TIC) (<0 to ~5 mM) at constant pH, so that ratios of CO2 and HCO3- remained relatively constant. Second, we varied pH (~8.54 to 7.52) at constant TIC, so that CO2 increased whilst HCO3- declined. We found that 14C-assimilation could be described by the same function of CO2 for both approaches, but it showed different dependencies on HCO3- when pH was varied at constant TIC than when TIC was varied at constant pH. A numerical model of the carbon-concentrating mechanism (CCM) of Trichodesmium showed that carboxylation rates are modulated by HCO3- and pH. The decrease in assimilation of inorganic carbon (Ci) at low CO2, when TIC was varied, was due to HCO3- uptake limitation of the carboxylation rate. Conversely, when pH was varied, Ci assimilation declined due to a high-pH mediated increase in HCO3- and CO2 leakage rates, potentially coupled to other processes (uncharacterised within the CCM model) that restrict Ci assimilation rates under high-pH conditions.

Predictions of response to temperature are contingent on model choice and data quality.

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.

A Key Marine Diazotroph in a Changing Ocean: The Interacting Effects of Temperature, CO2 and Light on the Growth of Trichodesmium erythraeum IMS101.

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.