H+ fluxes in phytoplankton - a mechanistic and modelling study of their physiological roles and impact upon community responses to ocean acidification
Lead Research Organisation:
Marine Biological Association of the United Kingdom
Department Name: Marine Biology
Abstract
The oceans remove about half of the carbon dioxide (CO2) that we release into the atmosphere and produce about half of the oxygen that we breathe. The photosynthetic marine phytoplankton play a major role in these processes, contributing to global carbon, nitrogen and sulphur cycling. Phytoplankton are not simply single-celled plants. They represent an extremely diverse collection of algae with many novel traits and complex evolutionary histories which are still poorly understood.
The increase in atmospheric carbon dioxide due to the burning of fossil fuels has major climatic implications. A result of the oceans absorbing much of this CO2 is the acidification of surface ocean waters - a drop from pH 8.2 to pH 7.7 is predicted by the end of the century. As ocean pH has remained stable for many millions of years this may have profound effects on many marine organisms that have not previously experienced this level of pH or rate of change during their recent evolutionary history. Ocean acidification will also change the levels of carbonate and nutrient ions, all of which may have significant impacts on the physiology of marine phytoplankton. While some of these impacts are being intensively studied, the direct effect of decreased pH itself on phytoplankton physiology has been largely overlooked.
Marine phytoplankton, like all organisms, must tightly regulate their cellular pH by in order to maintain favourable conditions for cellular processes. We have been studying mechanisms of pH regulation in coccolithophores, an important group of phytoplankton that play a major role in the global carbon cycle through their production of calcium carbonate scales (coccoliths) which sink to the deep ocean following cell death. We have discovered that coccolithophores use protein pores (channels) in their outer cell membrane to regulate pH inside the cell. These channels allow H+ to exit from the cell whenever acidity in the cell increases, thus acting to keep pH inside the cell constant. This is particularly important for coccolithophores as the production of coccoliths in the cell results in a constant production of H+ which need to be removed or the acidity inside of the cell would increase to dangerous levels. This novel mechanism is extremely sensitive to changes in external pH and may no longer function effectively at near future ocean pH levels. We have also found this form of H+ channel in diatoms, the most numerous and productive group of phytoplankton.
Remarkably, we have found that coccolithophore cells acclimated in the laboratory to growth at lower pH no longer appear to use a H+ channel. While this suggests coccolithophores may be able to cope with lower pH, we do not know the wider or long-term physiological implications of this mechanistic switch. This is clearly something we urgently need to understand.
This project will examine in detail the mechanisms of pH homeostasis in coccolithophores and diatoms. Our modelling studies predict that mechanisms of cellular pH regulation are likely to differ in large and small phytoplankton species as these will experience greatly different fluctuations in pH at the cell surface due to physical effects of cell size on diffusion at the cell surface. We propose that different mechanisms of pH homeostasis employed by phytoplankton species may play a major role in the response of these organisms to ocean acidification.
In order to gauge how these novel aspects of phytoplankton physiology will impact upon marine ecosystems on a broader scale, we will use modelling approaches to examine how cellular H+ fluxes in phytoplankton cells respond to changes in their environment. These mathematical models will enable us to predict the ranges of pH experienced by different phytoplankton species both currently and in the future and will allow us to evaluate their impact on the diversity of natural phytoplankton populations that will be studied in related programmes.
The increase in atmospheric carbon dioxide due to the burning of fossil fuels has major climatic implications. A result of the oceans absorbing much of this CO2 is the acidification of surface ocean waters - a drop from pH 8.2 to pH 7.7 is predicted by the end of the century. As ocean pH has remained stable for many millions of years this may have profound effects on many marine organisms that have not previously experienced this level of pH or rate of change during their recent evolutionary history. Ocean acidification will also change the levels of carbonate and nutrient ions, all of which may have significant impacts on the physiology of marine phytoplankton. While some of these impacts are being intensively studied, the direct effect of decreased pH itself on phytoplankton physiology has been largely overlooked.
Marine phytoplankton, like all organisms, must tightly regulate their cellular pH by in order to maintain favourable conditions for cellular processes. We have been studying mechanisms of pH regulation in coccolithophores, an important group of phytoplankton that play a major role in the global carbon cycle through their production of calcium carbonate scales (coccoliths) which sink to the deep ocean following cell death. We have discovered that coccolithophores use protein pores (channels) in their outer cell membrane to regulate pH inside the cell. These channels allow H+ to exit from the cell whenever acidity in the cell increases, thus acting to keep pH inside the cell constant. This is particularly important for coccolithophores as the production of coccoliths in the cell results in a constant production of H+ which need to be removed or the acidity inside of the cell would increase to dangerous levels. This novel mechanism is extremely sensitive to changes in external pH and may no longer function effectively at near future ocean pH levels. We have also found this form of H+ channel in diatoms, the most numerous and productive group of phytoplankton.
Remarkably, we have found that coccolithophore cells acclimated in the laboratory to growth at lower pH no longer appear to use a H+ channel. While this suggests coccolithophores may be able to cope with lower pH, we do not know the wider or long-term physiological implications of this mechanistic switch. This is clearly something we urgently need to understand.
This project will examine in detail the mechanisms of pH homeostasis in coccolithophores and diatoms. Our modelling studies predict that mechanisms of cellular pH regulation are likely to differ in large and small phytoplankton species as these will experience greatly different fluctuations in pH at the cell surface due to physical effects of cell size on diffusion at the cell surface. We propose that different mechanisms of pH homeostasis employed by phytoplankton species may play a major role in the response of these organisms to ocean acidification.
In order to gauge how these novel aspects of phytoplankton physiology will impact upon marine ecosystems on a broader scale, we will use modelling approaches to examine how cellular H+ fluxes in phytoplankton cells respond to changes in their environment. These mathematical models will enable us to predict the ranges of pH experienced by different phytoplankton species both currently and in the future and will allow us to evaluate their impact on the diversity of natural phytoplankton populations that will be studied in related programmes.
Planned Impact
This proposal aims to deliver substantial and lasting impact by providing mechanistic understanding of an essential process in marine phytoplankton. As this physiological process will be impacted by ocean acidification, the research will be of relevance to a wide variety of stakeholders with climate change interests. In addition to diverse scientific communities, the research will therefore have a wider impact in relation to understanding of processes and activities that are underpinned by marine productivity and the stability of marine ecosystems, from food production and tourism through to environmental management.
The proposed research is cutting edge blue-skies research aimed at gaining a better understanding of fundamental biogeochemical processes. The impact of the research on many of these diverse stakeholders may be indirect. Although we will engage directly with a variety of stakeholders (in academic, commercial and policy areas), a key goal of the proposed research is to build pathways to enable scientific breakthroughs at the organism level to feed through and inform stakeholders of the impacts at the ecosystem and ultimately global level. We aim to accomplish this by building cellular and ecosystem models to broaden the impact of our research and translate progress at the cellular level into meaningful impacts at the ecosystem level. Our aim is to enhance and facilitate the integration of scientific communities engaged in experimental and modelling approaches to promote the dissemination of blue skies research. This approach and its implementation are discussed in more detail in the Pathways to Impact attachment.
The economic and societal impacts of the research are broad as the results may affect many aspects of society that rely on marine ecosystems.
Non-academic stakeholders include policy forming bodies such as Governmental Environment and Climate Change Departments (e.g. the European Union, the UK Met Office, UK Government Departments, including DECC and DEFRA) as well as international bodies and NGOs (IPCC, environmental and fisheries charities, pressure groups). All of these groups have a potential interest in marine primary productivity and the impact ocean acidification may have on this process. Improved quantitative understanding of likely consequences of environmental change on novel physiological processes in marine phytoplankton will allow these policy forming bodies to address issues such as CO2 emission and mitigation strategies and policies. The research will also provide information that may be used in ecosystem management protection, and prediction and mitigation against any undesirable changes.
The proposed research is cutting edge blue-skies research aimed at gaining a better understanding of fundamental biogeochemical processes. The impact of the research on many of these diverse stakeholders may be indirect. Although we will engage directly with a variety of stakeholders (in academic, commercial and policy areas), a key goal of the proposed research is to build pathways to enable scientific breakthroughs at the organism level to feed through and inform stakeholders of the impacts at the ecosystem and ultimately global level. We aim to accomplish this by building cellular and ecosystem models to broaden the impact of our research and translate progress at the cellular level into meaningful impacts at the ecosystem level. Our aim is to enhance and facilitate the integration of scientific communities engaged in experimental and modelling approaches to promote the dissemination of blue skies research. This approach and its implementation are discussed in more detail in the Pathways to Impact attachment.
The economic and societal impacts of the research are broad as the results may affect many aspects of society that rely on marine ecosystems.
Non-academic stakeholders include policy forming bodies such as Governmental Environment and Climate Change Departments (e.g. the European Union, the UK Met Office, UK Government Departments, including DECC and DEFRA) as well as international bodies and NGOs (IPCC, environmental and fisheries charities, pressure groups). All of these groups have a potential interest in marine primary productivity and the impact ocean acidification may have on this process. Improved quantitative understanding of likely consequences of environmental change on novel physiological processes in marine phytoplankton will allow these policy forming bodies to address issues such as CO2 emission and mitigation strategies and policies. The research will also provide information that may be used in ecosystem management protection, and prediction and mitigation against any undesirable changes.
People |
ORCID iD |
Colin Brownlee (Principal Investigator) |
Publications
Bach LT
(2013)
Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi.
in The New phytologist
Brodie J
(2014)
The future of the northeast Atlantic benthic flora in a high CO2 world.
in Ecology and evolution
Brownlee C
(2015)
Coccolithophore biomineralization: New questions, new answers.
in Seminars in cell & developmental biology
Chrachri A
(2018)
Dynamic changes in carbonate chemistry in the microenvironment around single marine phytoplankton cells.
in Nature communications
De Vries J
(2021)
Haplo-diplontic life cycle expands coccolithophore niche
in Biogeosciences
Durak GM
(2016)
A role for diatom-like silicon transporters in calcifying coccolithophores.
in Nature communications
Durak GM
(2017)
The role of the cytoskeleton in biomineralisation in haptophyte algae.
in Scientific reports
Faktorová D
(2020)
Genetic tool development in marine protists: emerging model organisms for experimental cell biology.
in Nature methods
Flynn K
(2012)
Changes in pH at the exterior surface of plankton with ocean acidification
in Nature Climate Change
Flynn KJ
(2015)
Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession.
in Proceedings. Biological sciences
Description | The work showed that proton channels in the cell membrane of phytoplankton, particularly coccolithophores, were essential for the regulation of pH and, in calcifying phytoplankton, fro removing excess proton produced during the calcification reaction. The work generated the most detailed cellular model for transport processes underlying calcification to date. |
Exploitation Route | Mainly other academic users and biological oceanographic modellers |
Sectors | Environment |
Description | ERC Advanced Grant |
Amount | € 2,700,000 (EUR) |
Funding ID | 670390 |
Organisation | European Research Council (ERC) |
Sector | Public |
Country | Belgium |
Start | 10/2015 |
End | 10/2020 |
Description | Marine Microbial Initiative |
Amount | $156,550 (USD) |
Organisation | Gordon and Betty Moore Foundation |
Sector | Charity/Non Profit |
Country | United States |
Start | 11/2015 |
End | 11/2016 |
Description | Marine Microbial Initiative |
Amount | $250,000 (USD) |
Organisation | Gordon and Betty Moore Foundation |
Sector | Charity/Non Profit |
Country | United States |
Start | 01/2018 |
End | 01/2020 |
Description | NSF GEO NERC |
Amount | £600,000 (GBP) |
Funding ID | NE/N011708/1 |
Organisation | Natural Environment Research Council |
Sector | Public |
Country | United Kingdom |
Start | 10/2016 |
End | 10/2019 |
Description | BBSRC PHYCONET NIBB |
Organisation | Biotechnology and Biological Sciences Research Council (BBSRC) |
Country | United Kingdom |
Sector | Public |
PI Contribution | Membership of network. Workshop attendance |
Collaborator Contribution | Membership of network. Workshop attendance |
Impact | None to date |
Start Year | 2013 |
Description | USA scientific colllaboration |
Organisation | University of North Carolina Wilmington |
Country | United States |
Sector | Academic/University |
PI Contribution | Cellular and molecular physiology of haptophytes |
Collaborator Contribution | Electron microscopy and electrophysiology of coccolithophores, contributing essential data to major publication |
Impact | Publication (2016) in Nature Communications |
Description | 32nd Microelectrode Techniques Workshop |
Form Of Engagement Activity | Participation in an activity, workshop or similar |
Part Of Official Scheme? | No |
Geographic Reach | International |
Primary Audience | Professional Practitioners |
Results and Impact | 24 students and postdocs attended a 2-week practical workshop on single cell physiology. |
Year(s) Of Engagement Activity | Pre-2006,2006,2007,2008,2009,2010,2011,2012,2013,2014,2015,2016 |
URL | http://www.mba.ac.uk/microelectrode-techniques-for-cell-physiology/ |