Identifying the mechanisms and resource use implications of acclimation to high-temperature in marine cyanobacteria.

Lead Research Organisation: University of Essex
Department Name: Life Sciences

Abstract

Sea surface temperature has increased by about 0.8 degrees Celcius since 1880 and is projected to increase by another 2 degrees by the year 2100. This will expose the plants and animals that live in tropical waters to temperatures that are warmer than their ancestors have experienced over the past million years. Included in these organisms are the photosynthetic microrganisms that provide the organic matter that supports marine food webs and facilitate transfer of carbon dioxide from the atmosphere to ocean. In tropical waters where temperatures are above about 25 degrees Celcius, phytoplankton are likely to experience direct negative effects of increased temperature on their physiology as they are often exposed to temperatures that are higher than the optimal temperature for their growth. This situation contrasts with that for temperate and polar waters where increased temperature may stimulate growth of the indigenous phytoplankton species or allow more thermally tolerant species to immigrate.

Our research addresses the questions "How do cyanobacteria acclimate to temperatures that are supra-optimal for growth?" "What are the implications of this acclimation for their productivity in a warming ocean?" and "How can we account for acclimation to supra-optimal temperatures in models of cyanobacteria growth?" Unlike previous research on short-term (minutes to hours) responses of cyanobacteria, algae and vascular plants to heat shock, we propose to investigate the mechanisms of long-term (days to weeks) acclimation to heat stress and the implications of this acclimation for growth and physiology. As far as we are aware, this will be the first such investigation of long term acclimation to supra-optimal (heat) temperatures for an alga or a cyanobacterium, and as such will complement the more extensive literature on acclimation to sub-optimal (cold) temperatures in plants, algae and cyanobacteria by providing information that is particularly relevant in the face of global warming. We will employ a holistic approach using state-of-the-art methods to obtain this understanding. Transcriptomics will be used to generate the data to construct gene regulatory networks involved in sensing and responding to high temperature. Comparison of these networks amongst species with different tolerances to high temperature will be used to identify communalities and differences that may explain the observed thermal sensitivities. Proteomics and metabolomics will be used to assess the remodeling of cell metabolism that occurs as a consequence of acclimation to high temperature. Measurements of physiological rates, elemental composition (C, N, P) and biochemical composition will be used in an assessment of the system level outcomes of this acclimation in terms of biomass and productivity. The proposed comprehensive assessment of thermal acclimation is both timely and novel, and will contribute to continued excellence in a field where UK researchers make major impacts in a topic of global significance.

Our research will help scientists to understand how global warming due to man's activities is changing a fundamental component of Earth's life support system. Marine phytoplankton produce about 50% of the oxygen that we breathe, and play a role over millennial times scales in regulating atmospheric carbon dioxide levels. The information that we obtain will be used in the further development of the increasingly sophisticated models of marine ecology that are used in making projections of how the ocean is responding to climate change. In addition, cyanobacteria are being investigated for their potential use in biotechnology for production of low value products such as protein for animal feed or lipids for production of bio-diesel, as well as high value products including nutritional supplements (carotenoids, fatty acids, polysaccharides, vitamins, sterols) for consumption by humans and other products (dyes, pharmaceuticals, adhesives, surfactants).

Planned Impact

Who will benefit?

This is a blue skies proposal for which there are no immediate commercial or technological applications or specifically identifiable end users who should be involved during the execution of the project. However, we will achieve non-academic impact during the course of the project by engagement with the public.

In the longer term, the insights that we gain have the potential to inform new ocean ecosystem models for use in projecting the role of the oceans in climate change. Thus, amongst the benefits of this research will be a better understanding of how the Earth/climate system responds to global warming such as those that arise from the Met Office's ocean carbon cycle model (http://imarnet.org/Models/Hadley_Centre_Ocean_Carbon_Cycle_Model). Ultimately, this can have an impact on public policy after being fed into assessments of future climates such as those produced by the Intergovernmental Panel on Climate Change.

The outcomes of this research may also be able to be used to underpin translational research in the area of cyanobacterial biotechnology including cultivation of cyanobacteria for commercial biotechnological applications.

How will they benefit?

Engagement with the public. There is a strong public engagement in the U.K. with environmental matters that stems in part from the excellent natural history media industry in this country. The public will benefit as it will increase their knowledge about essential life forms that shape key processes on our planet such as carbon fixation and cycling of elements thus providing insights into how climate change impacts marine phytoplankton and the global carbon cycle.

Impacts on public policy. The potential impacts that this research can have on public policy in relation to climate change will be indirect. They will stem from the use of the phytoplankton growth models that we develop as part of this research by other scientists who formulate and apply ocean biogeochemical models in climate research. Geider has been and continues to be actively involved with the ocean modelling community research (e.g; Allen et al. 2010 Marine ecosystem models for earth systems applications. Journal of Marine Systems 81: 19-33). These models provide input to the Intergovernmental Panel on Climate Change and others in assessments of how climate is likely to change in response to anthropogenic forcing. Such model predictions inform policy decisions and public policy making particularly in responses to climate change. There is significant policy interest (e.g. in DEFRA) on carbon fluxes within water column and to benthic sediments to inform policy on carbon sequestration and national carbon inventories (http://www.defra.gov.uk/evidence/science/what/climate.htm) (http://www.defra.gov.uk/environment/marine/documents/science/marine-research.pdf).

Cyanobacterial biotechnology. Start-up teams and companies will potentially benefit from our research by obtaining new insights into how temperature affects the ability of cyanobacteria to grow and produce lipids, carbohydrates and proteins under non-optimal high-temperatures. A fundamental knowledge of the molecular biology and physiology of heat stress could contribute to optimizing algal strains for biofuel production and production of high-value end products such as polyunsaturated fatty acids. The new understanding of the gene regulatory networks involved in coping with and acclimation to thermal stress in cyanobacteria that will arise from this research may be useful in designing and genetically modifying cyanobacteria and microalgae so that they can better cope with temperature stress that may be experienced in closed system bioreactors. In addition, new insights into unique metabolites that are detected from our metabolomics experiments and/or better elucidation of the biosynthetic pathways and regulatory networks that may arise from use of our transcriptomics and metabolomics data.
 
Description The equations used to model the temperature dependence of phytoplankton growth rate and a variety of traits in other organisms across the full range of their temperature response, including supra- and suboptimal temperatures was evaluated. Although many equations have comparable abilities to fit data and equally high requirements for data quality (number of test temperatures and range of temperatures captured), they can lead to different estimates of the optimal temperature and thermal tolerance limits and optimal temperature. Consequently, biogeographic predictions based even the best-fitting models can exceed the global biological change predicted for ten years of global warming at current rates. Thus, studies of the biological response to global changes in temperature must carefully consider the model selected and the quality of the data used for parametrizing the model.

Improvements to Single Turnover Active Fluorometry (STAF) instrumentation and methodology that significantly increase the reliability of measurements of phytoplankton photosynthetic electron transfer rates (JVPII2 which is an index of gross primary production) were identified. Fluorescence based corrections for potential errors associated with both (1) baseline fluorescence and (2) pigment-packaging effect were identified and evaluated. For baseline ?uorescence, the correction incorporates an assumed consensus PSII photochemical ef?ciency for dark-adapted material. The error generated by the package effect can be minimized through the ratio of variable ?uorescence measured within narrow wavebands centered at 730 nm, where the re-absorption of PSII ?uorescence emission is minimal, and at 680 nm, where re-absorption of PSII ?uorescence emission is maximal.

The death rate due to heat stress was found to have little effect on population growth rates of two marine diatoms, Thalassiosira pseudonana and Phaeoactylum tricornutum, when temperatures was within the thermal tolerance limits of these species. This is contrary to a recent paper (Thomas et al 2017; Global Change Biology 23, 3269-3280), which interpreted the effect of temperature-nutrient interactions using a model of thermal performance that allowed for a significant exponential increase of death within increasing temperature rather than to a decline in the growth rate (cell division rate) at supra-optimal temperatures. In contrast, we found that the death rate varies little until temperature exceeds the upper thermal tolerance limit, but increases dramatically even when temperature at higher temperatures. This result has significant implications for how the thermal performance of growth rate is accounted for in biogeochemical and biogeographic models.

The competitive ability of two marine species, Phaeodactylum tricornutum and Thalassiosira pseudonana, along a temperature gradient (9-35°C) was investigated. Across this temperature gradient, the competitive outcomes under both nutrient-replete and nitrogen-limited conditions 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 species when measured in monocultures.

Other key findings await the completion of the data analysis and interpretation of transcriptomic, proteomic, metabolic, chemical and physiological data analysis for time series experiments to assess response to short term (<24 hour) heat stress on Synechocystis (PCC6803), Synechococcus (WH8103) and Phaeodactylum tricornutum (CCMP 2561, strain synonym CCAP 1055/1), and e full (steady-state growth) acclimation to sub-optimal, optimal, and supra-optimal temperatures Synechecoccus and P. tricornutum.
Exploitation Route The key findings regarding modelling thermal performance of phytoplankton growth necessitate a reevaluation of the suitability of existing data on the temperature dependence of phytoplankton growth for making inference about phytoplankton biogeography. They also provide guidance on data requirements for new experiments into the thermal performance of phytoplankton growth.

The key findings related to use of STAF to assess phytoplankton primary production have already been employed in the design of improved instrumentation, in part by providing data that was used as proof of concept for NERC grant (NE/PO208441). Reliable STAF estimates of JVPII provided by new instrumentation can take us signi?cantly closer to achieving the objective of obtaining reliable autonomous estimates of PhytoPP, especially if used in conjunction with simultaneous satellite measurements of ocean color.

The key finding regarding the temperature dependence of death rate for two species needs to be extended to other species from a range of higher taxonomic groups of phytoplankton. Similar experiments need to be conducted to assess the interactions of temperature with light intensity and nutrient limitation to assess the extent to which population growth rates are directly or indirectly affected by temperature dependence of cell division and mortality rates.

The key finding regarding how mixed populations respond to abiotic changes is required to adequately predict how environmental changes such as warming may affect the future composition of phytoplankton communities, which can in turn affect marine food webs and ocean biogeochemistry. The ability to determine the competitive outcomes from physiological responses of single species to environmental changes has the potential to significantly improve the predictive power of models of phytoplankton spatial distribution and community composition models.
Sectors Environment

 
Description Improvements to Single Turnover Active Fluorescence (STAF) approach to measuring gross phytoplankton primary production described in Boatman et al (2019; Front. Mar. Sci. 6:319. doi: 10.3389/fmars.2019.00319) contributed to the design specifications for new STAF equipment developed as part of NERC grant NE/PO208441 by a UK company. Use of the new instrumentation has the potential to achieve societal impacts if used to document changes in key ocean variable, primary production, in response to changes that may be attributable to global warming and/or marine pollution.
First Year Of Impact 2019
Sector Environment
Impact Types Economic

 
Description Project website 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact A bespoke website describing the general background, objectives, approaches and make-up of the team undertaking the project was constructed and uploaded. Results of the research will be posted as and when they become available.
Year(s) Of Engagement Activity 2018
URL http://geiderlab.com
 
Description Research experience for undergraduate life sciences student. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact A University of Essex funded one month Undergraduate Research Experience Placement (UROP) for a 1st year undergraduate student, The student gained valuable work experience as a research technician by designing and conducting an experiment on the effect of temperature on photosynthesis of marine cyanobacteria. Cyanobacteria play important roles in photosynthesis and nitrogen fixation, two key biological processes upon which life depends.
Year(s) Of Engagement Activity 2017