H+ fluxes in phytoplankton - a mechanistic and modelling study of their physiological roles and impact upon community responses to ocean acidification

Lead Research Organisation: Plymouth Marine Laboratory
Department Name: Plymouth Marine Lab

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.

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.
 
Description We have examined how phytoplankton regulate their pH. pH regulation is a vital aspect of metabolism that underpins central metabolic processes such as photosynthesis. We have found significant differences between different groups of phytoplankton that might result in differences in their ability to adapt to future changes in ocean pH.
Using tiny pH meters, we have also identified how seawater pH fluctuates in the microenvironment around large and small phytoplankton cells. We have been able to perform the first simultaneous measurements of pH and carbonate (CO32-) around a single phytoplankton cell. We have demonstrated significant effects of metabolic processes on seawater carbonate chemistry surrounding phytoplankton that help us understand how these cells take up carbon from seawater for photosynthesis and how cell size constrains their physiology.
Exploitation Route The results will have important impacts for how phytoplankton respond to a changing environment. For academic users this will stimulate further research into phytoplankton physiology. For non-academic users the results will inform us about potential constraints and changes to phytoplankton communities, which may impact marine food webs.
Sectors Energy,Environment,Leisure Activities, including Sports, Recreation and Tourism,Manufacturing, including Industrial Biotechology

 
Description The research grant has yielded very exciting results, published in Nature Communications (Jan 2018). There have been no economic or societal benefits yet, although we expect that they will be some in the future relating to the Environment and Industrial Biotech sectors
First Year Of Impact 2018
Sector Environment,Manufacturing, including Industrial Biotechology