Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton

Understanding the mechanisms that determine how phytoplankton adapt to warming will substantially improve the realism of models describing ecological and biogeochemical effects of climate change. Here, we quantify the evolution of elevated thermal tolerance in the phytoplankton, Chlorella vulgaris. Initially, population growth was limited at higher temperatures because respiration was more sensitive to temperature than photosynthesis meaning less carbon was available for growth. Tolerance to high temperature evolved after ≈ 100 generations via greater down-regulation of respiration relative to photosynthesis. By down-regulating respiration, phytoplankton overcame the metabolic constraint imposed by the greater temperature sensitivity of respiration and more efficiently allocated fixed carbon to growth. Rapid evolution of carbon-use efficiency provides a potentially general mechanism for thermal adaptation in phytoplankton and implies that evolutionary responses in phytoplankton will modify biogeochemical cycles and hence food web structure and function under warming. Models of climate futures that ignore adaptation would usefully be revisited

On the community and ecosystem level consequences of warming

PhDThe carbon cycle modulates climate change, via the regulation of atmospheric CO2, and it represents one of the most important ecosystem services of value to humans. However, considerable uncertainties remain concerning potential feedbacks between the biota and the climate. I used an ecosystem-level manipulative experiment in freshwater mesocosms to test novel theoretical predictions derived from the metabolic theory of ecology (MTE), in an attempt to understand the consequences of warming for aquatic communities and ecosystems. The yearlong experiment simulated a warming scenario (A1B) expected by the end of the century. The experiment revealed that (1) Ecosystem respiration increased at a faster rate than primary production, reducing carbon sequestration by 13%. These results confirmed my theoretical predictions based on the different activation energies of these two processes. Furthermore, I provided a theoretical prediction that accurately quantified the precise magnitude of the reduction in carbon sequestration observed experimentally, based simply on the activation energies of these metabolic processes and the relative increase in temperature. (2) Methane efflux increased at a faster rate than ecosystem respiration and photosynthesis in response to temperature. This phenomenon was well described by the activation energies of these metabolic processes. Therefore, warming increased the fraction of primary production emitted as methane by 21%, and methane efflux represented a 9% greater fraction of ecosystem respiration. Moreover, because methane is 21 times more potent as a greenhouse gas, relative to CO2, this work suggests that warming may increase the greenhouse gas efflux potential of freshwater ecosystems, revealing a previously unknown positive feedback between warming and the carbon cycle. (3) Warming benefited smaller organisms and increased the steepness of the slope of the 3 community size spectrum. As a result the mean body size of phytoplankton in the warmed systems decreased by an order of magnitude. These results were down to a systematic shift in phytoplankton community composition in response to warming. Furthermore, warming reduced community biomass and total phytoplankton biomass, although zooplankton biomass was unaffected. This resulted in an increase in the zooplankton to phytoplankton biomass ratio in the warmed mesocosms, which could be explained by faster turnover within the phytoplankton assemblages. Warming therefore shifted the distribution of phytoplankton body size towards smaller individuals with rapid turnover and low standing biomass, resulting in a reorganisation of the biomass structure of the food webs. The results of this thesis suggest that as freshwater ecosystems warm they become increasingly carbon limited, resulting in a reduced capacity for carbon sequestration, elevated greenhouse gas efflux potential, and altered body size and biomass distribution

On the community and ecosystem level consequences of warming

Memoria de tesis doctoral presentada por Gabriel Yvon-Durocher para obtener el título de Doctor en Philosophy por la Queen Mary University of London (QMUL), realizada bajo la dirección de la Dr. José María Montoya del Institut de Ciències del Mar (ICM-CSIC).-- 173 pages, 6 appendicesThe carbon cycle modulates climate change, via the regulation of atmospheric CO2, and it represents one of the most important ecosystem services of value to humans. However, considerable uncertainties remain concerning potential feedbacks between the biota and the climate. I used an ecosystem-level manipulative experiment in freshwater mesocosms to test novel theoretical predictions derived from the metabolic theory of ecology (MTE), in an attempt to understand the consequences of warming for aquatic communities and ecosystems. [...]Peer Reviewe

Modelling ecosystem adaptation and dangerous rates of global warming

This is the author accepted manuscript. The final version is available from Portland Press via the DOI in this recordWe are in a period of relatively rapid climate change. This poses challenges for individual species and threatens the ecosystem services that humanity relies upon. Temperature is a key stressor. In a warming climate, individual organisms may be able to shift their thermal optima through phenotypic plasticity. However, such plasticity is unlikely to be sufficient over the coming centuries. Resilience to warming will also depend on how fast the distribution of traits that define a species can adapt through other methods, in particular through redistribution of the abundance of variants within the population and through genetic evolution. In this paper, we use a simple theoretical ‘trait diffusion’ model to explore how the resilience of a given species to climate change depends on the initial trait diversity (biodiversity), the trait diffusion rate (mutation rate), and the lifetime of the organism. We estimate theoretical dangerous rates of continuous global warming that would exceed the ability of a species to adapt through trait diffusion, and therefore lead to a collapse in the overall productivity of the species. As the rate of adaptation through intraspecies competition and genetic evolution decreases with species lifetime, we find critical rates of change that also depend fundamentally on lifetime. Dangerous rates of warming vary from 1°C per lifetime (at low trait diffusion rate) to 8°C per lifetime (at high trait diffusion rate). We conclude that rapid climate change is liable to favour short-lived organisms (e.g. microbes) rather than longer-lived organisms (e.g. trees).University of ExeterCSSP-Brazi

Evolutionary temperature compensation of carbon fixation in marine phytoplankton

The efficiency of carbon sequestration by the biological pump could decline in the coming decades because respiration tends to increase more with temperature than photosynthesis. Despite these differences in the short-term temperature sensitivities of photosynthesis and respiration, it remains unknown whether the long-term impacts of global warming on metabolic rates of phytoplankton can be modulated by evolutionary adaptation. We found that respiration was consistently more temperature dependent than photosynthesis across 18 diverse marine phytoplankton, resulting in universal declines in the rate of carbon fixation with short-term increases in temperature. Long-term experimental evolution under high temperature reversed the short-term stimulation of metabolic rates, resulting in increased rates of carbon fixation. Our findings suggest that thermal adaptation may therefore have an ameliorating impact on the efficiency of phytoplankton as primary mediators of the biological carbon pump

Linking phytoplankton community metabolism to the individual size distribution

This is the final version of the article. Available from the publisher via the DOI in this recordQuantifying variation in ecosystem metabolism is critical to predicting the impacts of environmental change on the carbon cycle. We used a metabolic scaling framework to investigate how body size and temperature influence phytoplankton community metabolism. We tested this framework using phytoplankton sampled from an outdoor mesocosm experiment, where communities had been either experimentally warmed (+ 4 °C) for 10 years or left at ambient temperature. Warmed and ambient phytoplankton communities differed substantially in their taxonomic composition and size structure. Despite this, the response of primary production and community respiration to long- and short-term warming could be estimated using a model that accounted for the size- and temperature dependence of individual metabolism, and the community abundance-body size distribution. This work demonstrates that the key metabolic fluxes that determine the carbon balance of planktonic ecosystems can be approximated using metabolic scaling theory, with knowledge of the individual size distribution and environmental temperature.NERC. Grant Number: PASW06

Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom

This is the final version of the article. Available from Springer Nature via the DOI in this recordThe publisher correction to this article is in ORE at: http://hdl.handle.net/10871/34487Diatoms contribute roughly 20% of global primary production, but the factors determining their ability to adapt to global warming are unknown. Here we quantify the capacity for adaptation to warming in the marine diatom Thalassiosira pseudonana. We find that evolutionary rescue under severe (32 °C) warming is slow, but adaptation to more realistic scenarios where temperature increases are moderate (26 °C) or fluctuate between benign and severe conditions is rapid and linked to phenotypic changes in metabolic traits and elemental composition. Whole-genome re-sequencing identifies genetic divergence among populations selected in the different warming regimes and between the evolved and ancestral lineages. Consistent with the phenotypic changes, the most rapidly evolving genes are associated with transcriptional regulation, cellular responses to oxidative stress and redox homeostasis. These results demonstrate that the evolution of thermal tolerance in marine diatoms can be rapid, particularly in fluctuating environments, and is underpinned by major genomic and phenotypic change.This study was funded by a Leverhulme Trust research grant (RPG-2013-335). Whole genome re-sequencing was carried out at Exeter Sequencing Service and Computational core facilities at the University of Exeter, where Dr. Karen Moore, Dr. Audrey Farbos, Paul O’Neill, and Dr. Konrad Paszkiewicz lead the handling of the samples. Exeter Squencing Services are supported by Medical Research Council Clinical Infrastructure award (MR/M008924/1), Wellcome Trust Institutional Strategic Support Fund (WT097835MF), Wellcome Trust Multi User Equipment Award (WT101650MA), and BBSRC LOLA award (BB/K003240/1)

Publisher Correction: Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom

The article for which this is the publisher correction is in ORE at: http://hdl.handle.net/10871/32652The PDF version of this Article was updated shortly after publication following an error which resulted in the Φ symbol being omitted from the left hand side of equation 8. The HTML version was correct from the time of publication

Community-level respiration of prokaryotic microbes may rise with global warming

Understanding how the metabolic rates of prokaryotes respond to temperature is fun-damental to our understanding of how ecosystem functioning will be altered by climatechange, as these micro-organisms are major contributors to global carbon efflux. Ecologicalmetabolic theory suggests that species living at higher temperatures evolve higher growthrates than those in cooler niches due to thermodynamic constraints. Here, using a globalprokaryotic dataset, we find that maximal growth rate at thermal optimum increases withtemperature for mesophiles (temperature optima.45◦C), but not thermophiles (&45◦C).Furthermore, short-term (within-day) thermal responses of prokaryotic metabolic rates aretypically more sensitive to warming than those of eukaryotes. Because climatic warmingwill mostly impact ecosystems in the mesophilic temperature range, we conclude that asmicrobial communities adapt to higher temperatures, their metabolic rates and therefore,biomass-specific CO2production, will inevitably rise. Using a mathematical model, weillustrate the potential global impacts of these findings