![Temperature variations in a raceway pond located in New ZeandRaceway pond (A) and associated temperature variations (B) during August 2013 (adapted from Béchet et al. [2011]). Experimental data are marked in red whereas the blue line corresponds to a dedicated model.](https://www.researchgate.net/profile/Ghjuvan-Micaelu-Grimaud/publication/305700643/figure/fig1/AS:613890614362118@1523374336127/Temperature-variations-in-a-raceway-pond-located-in-New-ZeandRaceway-pond-A-and_Q320.jpg)
![Dallinger experiment-Experiment conducted by Dallinger [1887] on the three monads Tetramitus rostratus, Monas dallingeri, Dallingera drysdali (adapted from Julou [2011]).](https://www.researchgate.net/profile/Ghjuvan-Micaelu-Grimaud/publication/305700643/figure/fig2/AS:613890614386688@1523374336184/Dallinger-experiment-Experiment-conducted-by-Dallinger-1887-on-the-three-monads_Q320.jpg)
![Adaptation of the thermal growth curve-Different hypotheses for the deformation of the thermal growth curve during thermal adaptation. A, horizontal-shift, B, hotter is better, C, specialist-generalist trade-off, D, hotter is broader and better, E, asymmetric adaptation. Adapted from Knies et al. [2009].](https://www.researchgate.net/profile/Ghjuvan-Micaelu-Grimaud/publication/305700643/figure/fig3/AS:613890614382602@1523374336222/Adaptation-of-the-thermal-growth-curve-Different-hypotheses-for-the-deformation-of-the_Q320.jpg)
![Selectiostat culture device-Culture of Tisochrysis lutea in the 'selectiostat' device. Adapted from Bonnefond [2015].](https://www.researchgate.net/profile/Ghjuvan-Micaelu-Grimaud/publication/305700643/figure/fig4/AS:613890614390796@1523374336240/Selectiostat-culture-device-Culture-of-Tisochrysis-lutea-in-the-selectiostat-device_Q320.jpg)
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Modelling the temperature effect on phytoplankton: from acclimation to adaptation
Abstract and Figures
Unicellular photosynthetic organisms forming the phytoplankton are the basis of primary production. Because these organisms cannot regulate their inner temperature, the medium temperature strongly constrains their growth. Understanding the impact of this factor is topical in a global change context. In this PhD thesis we have investigated how phytoplankton adapts to temperature. By analyzing the growth rate as a function of temperature for hundreds of species we highlighted the characteristics that can be accurately described by a mathematical model. We have identied the links between the cardinal temperatures as well as their thermodynamical fundament using the mechanistic Hinshelwood model. We then challenged the Eppley hypothesis `hotter is faster' for 5 phylogenetic phytoplankton groups and determined the evolutionary limits for each of them. We have also studied the adaptation mechanisms associated to long term temperature variations by developing an evolutionary model using the adaptive dynamics theory allowing to predict the evolutionary outcome of species adaptation to a simple temperature cycle. Our results have been compared to a selection experiment carried out in a controlled device on Tisochrysis lutea. Our method has been extended to predict the adaptation of a strain to periodic temperature profiles and study phytoplankton adaptation at the global ocean scale. In situ data of sea surface temperature have been used as a forcing variable and have permitted to show that the elevation of temperature will be critical for several species in particular for those living in areas where the annual temperature fluctuation is high such as the Mediterranean sea.
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... The optimal growth response envelope [45] for the whole Micromonas genus was calculated with a BR curve calibrated on a data set consisting in 57 couples (T opt , μ opt ) from the eleven experimental strains and the 46 collection strains. Moreover, the decreasing part of the curve was constrained with 8 couples (T, μ(T)) simulated from the M. commoda Warm thermotype model for temperatures equally distributed in the (T opt , T max ) interval for this thermotype. ...
... We constrained T Ã min;i and T Ã max;i by the envelope curve [45] of the Micromonas genus (Fig. 2b) that represents its evolution boundaries. ...
... b Average growth response to temperature for each phylogenetic group computed from 100,000 possible response curves simulated within the ranges observed in each phylogenetic group. The black line represents the overall, optimal growth response envelope [45] of Micromonas computed as μ opt vs. T opt , where μ opt and T opt are given by the average response of each thermotype. The grey shaded area is the standard deviation around μ opt the related thermal responses (see Methods). ...
Photosynthetic picoeukaryotes in the genus Micromonas show among the widest latitudinal distributions on Earth, experiencing large thermal gradients from poles to tropics. Micromonas comprises at least four different species often found in sympatry. While such ubiquity might suggest a wide thermal niche, the temperature response of the different strains is still unexplored, leaving many questions as for their ecological success over such diverse ecosystems. Using combined experiments and theory, we characterize the thermal response of eleven Micromonas strains belonging to four species. We demonstrate that the variety of specific responses to temperature in the Micromonas genus makes this environmental factor an ideal marker to describe its global distribution and diversity. We then propose a diversity model for the genus Micromonas, which proves to be representative of the whole phytoplankton diversity. This prominent primary producer is therefore a sentinel organism of phytoplankton diversity at the global scale. We use the diversity within Micromonas to anticipate the potential impact of global warming on oceanic phytoplankton. We develop a dynamic, adaptive model and run forecast simulations, exploring a range of adaptation time scales, to probe the likely responses to climate change. Results stress how biodiversity erosion depends on the ability of organisms to adapt rapidly to temperature increase.
... The model has been validated on temperature and nutrient experiments conducted with the phytoplankton diatom species Thalassiosira pseudonana (Thomas et al. 2017). Grimaud (2016) has developed a dynamical model taking into account temperature and nutrient for eukaryotes phytoplankton species, based on the Droop model (1968). In balanced-growth conditions, the model gives the following thermal growth curve: ...
... It is worth noting that we did not describe adaptation models at the evolutionary time-scale which are needed to understand long time effects of an increase in temperature on the thermal response. These models, mostly based on the adaptive dynamics theory, are currently being developed Grimaud 2016) and should be the next stage to understand the effect of global warming on oceans. ...
... The blue and red dashed lines correspond to the positive and negative terms of Eq. 40, respectively. b Model ofGrimaud (2016). Blue and red dashed lines correspond to / 1 ðTÞ and / 2 ðTÞ of Eq. ...
Phytoplankton are key components of ecosystems. Their growth is deeply influenced by temperature. In a context of global change, it is important to precisely estimate the impact of temperature on these organisms at different spatial and temporal scales. Here, we review the existing deterministic models used to represent the effect of temperature on microbial growth that can be applied to phytoplankton. We first describe and provide a brief mathematical analysis of the models used in constant conditions to reproduce the thermal growth curve. We present the mechanistic assumptions concerning the effect of temperature on the cell growth and mortality, and discuss their limits. The coupling effect of temperature and other environmental factors such as light are then shown. Finally, we introduce the models taking into account the acclimation needed to thrive with temperature variations. The need for new thermal models, coupled with experimental validation, is argued.
... Host growth and degradation In line with the work of Grimaud (2016), we used the Hinshelwood model (Hinshelwood 1946) to represent the impact of temperature on gross phytoplankton growth (μ) and nonlysis mortality (ψ) rates as follows: ...
... Four empirical parameters accurately represented this function (Bernard & Rémond 2012): the optimal growth temperature T μ opt at which growth is maximal (μ ¼ μ opt ), and the minimal and maximal temperatures of growth (T μ min and T μ max respectively). We express parameters from the Hinshelwood model according to Grimaud (2016): ...
Marine viruses interact with microbial hosts in dynamic environments shaped by variation in abiotic factors, including temperature. However, the impacts of temperature on viral infection of phytoplankton are not well understood. Here we coupled mathematical modelling with experiments to explore the effect of temperature on virus‐phytoplankton interactions. Our model shows the negative consequences of high temperatures on infection and suggests a temperature‐dependent threshold between viral production and degradation. Modelling long‐term dynamics in environments with different average temperatures revealed the potential for long‐term host‐virus coexistence, epidemic free or habitat loss states. We generalised our model to variation in global sea surface temperatures corresponding to present and future seas and show that climate change may differentially influence virus‐host dynamics depending on the virus‐host pair. Temperature‐dependent changes in the infectivity of virus particles may lead to shifts in virus‐host habitats in warmer oceans, analogous to projected changes in the habitats of macro‐, microorganisms and pathogens. The impacts of temperature on viral infection of phytoplankton are not well understood. Here we coupled mathematical modelling with experimental data sets to explore the effect of temperature on virus‐phytoplankton dynamics. Our model shows the negative consequences of high temperatures on infection and suggests a temperature‐dependent threshold between viral production and degradation. Our study suggests that ocean warming may lead to shifts in virus‐host habitats in future oceans, analogous to projected changes in the habitats of macroorganisms, microorganisms and pathogens.
Detailed comparison of growth kinetics at temperatures below and above the optimal temperature was carried out with Escherichia coli ML 30 (DSM 1329) in continuous culture. The culture was grown with glucose as the sole limiting source of carbon and energy (100 mg liter(-1) in feed medium), and the resulting steady-state concentrations of glucose were measured as a function of the dilution rate at 17.4, 28.4, 37, and 40 degrees C. The experimental data could not be described by the conventional Monod equation over the entire temperature range, but an extended form of the Monod model [mu = mu(max) x (s - s(min))/(Ks + s - s(min))], which predicts a finite substrate concentration at 0 growth rate (s(min)), provided a good fit. The two parameters mu(max) and s(min) were temperature dependent, whereas, surprisingly, fitting the model to the experimental data yielded virtually identical Ks values (approximately 33 microg liter(-1)) at all temperatures. A model that describes steady-state glucose concentrations as a function of temperature at constant growth rates is presented. In similar experiments with mixtures of glucose and galactose (1:1 mixture), the two sugars were utilized simultaneously at all temperatures examined, and their steady-state concentrations were reduced compared with to growth with either glucose or galactose alone. The results of laboratory-scale kinetic experiments are discussed with respect to the concentrations observed in natural environments.
The Isochrysidaceae is a family of non-calcifying organisms within the haptophyte order Isochrysidales. Isochrysis galbana, a species widely used as a food source in aquaculture, is the best-known representative of this family that contains three genera but only six described species. We sequenced partial nuclear small subunit (SSU) and large subunit rDNA and mitochondrial cytochrome oxidase 1 genes of 34 isochrysidacean culture strains (including authentic strains when available) and compared molecular phylogenetic inferences with cytological and ultrastructural observations. The isochrysidaceaen culture strain Isochrysis affinis galbana (Tahiti isolate), widely used in aquaculture and commonly known as T-Iso, is clearly genetically distinct from Isochrysisgalbana, despite seemingly being morphologically identical. A strain with a similar ultrastructure to that of Isochrysis galbana except for the lack of body scales had sequences that were more similar to but still distinct from those of Isochrysis galbana. Dicrateria inornata, a species that lacks body scales, is classified within the Isochrysidaceae, but the SSU rDNA sequence of the authentic strain of this species matches that of Imantonia rotunda within another haptophye order, the Prymnesiales. D. inornata and Imantonia rotunda have similar ultrastructure except for the respective absence/presence of scales. These results lead us to propose the erection of one new genus (Tisochrysis gen. nov.) and two new species (Tisochrysis lutea sp. nov. and Isochrysis nuda sp. nov.). D. inornata is reclassified within the Prymnesiales, and Imantonia rotunda is transferred to this genus (Dicrateria rotunda comb. nov.).
Temperature has a profound effect on the species composition and physiology of marine phytoplankton, a polyphyletic group of microbes responsible for half of global primary production. Here we ask whether and how thermal reaction norms in a key calcifying species, the coccolithophore Emiliania huxleyi, change as a result of 2.5 years of experimental evolution to a temperature ≈2°C below its upper thermal limit. Replicate experimental populations derived from a single genotype isolated from Norwegian coastal waters were grown at two temperatures for 2.5 yrs before assessing thermal responses at 6 temperatures from 15-26°C, with pCO2 (400/1100/2200 μatm) as a fully factorial additional factor. The two selection temperatures (15°/26.3°C) led to a marked divergence of thermal reaction norms. Optimal growth temperatures were 0.7°C higher in experimental populations selected at 26.3°C than those selected at 15.0°C. An additional negative effect of high pCO2 on maximal growth rate (8% decrease relative to lowest level) was observed. Finally, the maximum persistence temperature (Tmax) differed by 1-3°C between experimental treatments, as a result of an interaction between pCO2 and the temperature selection. Taken together, we demonstrate that several attributes of thermal reaction norms in phytoplankton may change faster than the predicted progression of ocean warming. This article is protected by copyright. All rights reserved.
Le monde fait face à une crise environnementale sans précédent, induite par l’action toujours plus marquée de l’homme sur son milieu. Depuis le début de l’ère industrielle, l’utilisation massive des énergies fossiles, a provoqué un dérèglement climatique planétaire. Les microalgues offrent la possibilité de produire des biocarburants avec une empreinte carbone réduite mais nécessitent encore de nombreuses améliorations pour être économiquement viables. Une de ces améliorations, à l’instar de l’agriculture moderne, réside dans la sélection de souches plus productives. Dans ce travail de thèse, nous avons développé la sélection par pression continue, consistant à utiliser les processus de l’évolution pour faire émerger des populations d’intérêt.Une première voie explorée a consisté à utiliser la température, paramètre crucial de la croissance des microalgues, comme moteur de sélection. En soumettant une culture à des variations diurnes de température durant une année, nous sommes parvenus à adapter une souche de Tisochrysis lutea à une gamme de températures plus large, la rendant donc plus tolérante aux variations de ce paramètre.La seconde voie a cherché à accroitre la capacité de Cylindrotheca closterium à emmagasiner ou au contraire à mobiliser son azote intracellulaire, propriété physiologiquement liée à sa capacité à produire des lipides. En forçant une population de microalgues à s'adapter à des apports discontinus d'azote (succession d'états de satiété et de carence), il a été possible de sélectionner les individus les plus riches en lipides.Enfin, nous avons modifié l'appareil pigmentaire de Tisochrisis lutea pour la rendre plus transparente à la lumière. En soumettant cette espèce à une succession de chocs lumineux, il a été possible de sélectionner les individus possédant les antennes photosynthétiques les plus petites, permettant une productivité accrue.
Groups of replicated lines of the bacterium Escherichia coli were propagated for 2,000 generations at constant 32, 37, or 42°C, or in an environment that alternated between 32 and 42°C. Here, we examine the performance of each group across a temperature range of 12-44°C measuring the temperatures over which each line can maintain itself in serial dilution culture (the thermal niche). Thermal niche was not affected by selection history: average lower and upper limits remained about 19 and 42°C for all groups. In addition, no significant differences among groups were observed in rate of extinction at more extreme temperatures. Within the thermal niche, we measured the mean fitness of the evolved groups relative to their common ancestor. Increases in mean fitness were temperature specific, with the largest increase for each group occurring near its selected temperature. Thus, the temperature at which mean fitness relative to the ancestor was greatest (the thermal optimum) diverged by about 10°C for the groups selected at constant 32°C versus constant 42°C. Tradeoffs in relative fitness (decrements relative to the ancestor elsewhere within the thermal niche) did not necessarily accompany fitness improvements, although tradeoffs were observed for a few of the lines. We conclude that adaptation in this system was quite temperature specific, but substantial divergence among groups in thermal optima had little effect on the limits of their thermal niches and did not necessarily involve tradeoffs in fitness at other temperatures.
Temperature provides a powerful theme for exploring environmental adaptation at all levels of biological organization, from molecular kinetics to organismal fitness to global biogeography. First, the thermodynamic properties that underlie biochemical kinetics and protein stability determine the overall thermal sensitivity of rate processes. Consequently, a single quantitative framework can assess variation in thermal sensitivity of ectotherms in terms of single amino acid substitutions, quantitative genetics, and interspecific differences. Thermodynamic considerations predict that higher optimal temperatures will result in greater maximal fitness at the optimum, a pattern seen both in interspecific comparisons and in within‐population genotypic variation. Second, the temperature‐size rule (increased developmental temperature causes decreased adult body size) is a common pattern of phenotypic plasticity in ectotherms. Mechanistic models can correctly predict the rule in some taxa, but lab and field studies show that rapid evolution can weaken or even break the rule. Third, phenotypic and evolutionary models for thermal sensitivity can be combined to explore potential fitness consequences of climate warming for terrestrial ectotherms. Recent analyses suggest that climate change will have greater negative fitness consequences for tropical than for temperate ectotherms, because many tropical species have relatively narrow thermal breadths and smaller thermal safety margins.