Diatom Sensory Mechanisms: Drivers of Global Marine Productivity

The oceans support a large proportion of global biodiversity. Sustaining life at the base of marine food chains are photosynthetic microbes, known collectively as phytoplankton. These organisms are vital in regulating our climate, absorbing carbon dioxide from the atmosphere. They also generate almost half the oxygen we breathe. Phytoplankton are probably best known for their formation of massive 'algal blooms' in the ocean, due to rapid population growth triggered by a combination of physical and biological factors. Due to the release of harmful toxins, some phytoplankton blooms can have a negative impact on marine ecosystems, fisheries and human health. Effects of climate change and nutrient pollution have led to more severe and frequent blooms. However, many blooms are not caused by harmful species, and are vital for sustaining marine ecosystems including fish populations. To better understand factors that control bloom dynamics and toxicity, we need to learn more about the molecular processes that trigger their sudden proliferation, and subsequent demise.

In many parts of the ocean, nutrients such as nitrogen and phosphorus are in scarce supply. This can limit phytoplankton growth, and cause competition between microbes for survival. In the marine environment a combination of physical factors can lead to sporadic increases in nutrients. This is one of the factors that can stimulate rapid proliferation of phytoplankton cells and lead to algal bloom formation. One of the most successful phytoplankton groups in modern oceans is the diatoms. Diatoms are particularly good at detecting favourable conditions and are often the first to dominate the early stages of bloom formation. Moreover, their success in regions of pulsed nutrient supply suggests that they possess sophisticated mechanisms for sensing and responding to fluctuations in nutrients. However, the sensory mechanisms that mediate the cellular responses of diatom cells to key environmental stimuli remain poorly understood. This represents a major knowledge gap, especially since it is the signalling mechanisms that coordinate acclimation to the environment that likely underpin the ecological success and global impact of the diatoms.

I have generated a cutting-edge toolkit to study how diatoms are able to sense changes in their environment using the signalling molecule calcium, which functions as a messenger within the cell. This has led to the remarkable discovery that diatoms use calcium for detecting pulses of the nutrient phosphorus. This novel nutrient signalling mechanism is distinct from plants and animals and points to fundamental differences in nutrient perception between these organisms, which need to be elucidated. I will dissect specific components of this signalling pathway to identify how it helps diatoms respond rapidly to changing nutrient conditions and contribute towards bloom formation. Using my innovative tools, I will also examine other unknown aspects of the diatom sensory system. Alongside physical factors, biological interactions of diatoms with other microbes such as competitors, parasites and predators can critically regulate their growth and bloom development. In the second part of my proposal I will examine how diatoms are able to sense, and alter their behaviour to interact with, their microbial neighbours. Since both nutrient supply and bacteria can govern toxin production by harmful diatoms, a key objective will be to expand my molecular tool kit to the toxic bloom-forming diatom Pseudo-nitzschia multiseries.

This research will identify mechanisms that govern dynamics of a globally important phytoplankton group that supports some of our major marine resources. The work will moreover provide insight of regulatory processes and 'master-regulators' that coordinate cellular responses to key environmental drivers that impact diatom growth and toxicity of harmful diatom species, allowing us to better predict bloom formation and toxicity.

The research proposed is both innovative and exciting, using cutting edge single-cell approaches to unlock phytoplankton signalling mechanisms that control cellular responses to key environmental drivers that likely underpin the ecological success and impact of a globally important group of phytoplankton, the diatoms. There are several societal/economic impacts of this work. In particular the research will have a wide impact in areas that are underpinned by marine productivity and the stability of marine ecosystems, from food production and tourism through to environmental management, alongside biotechnology and industry, as outlined below:

Marine policy:

Algal blooms are caused by excessive growth of algae, which can release harmful toxins, and have damaging effects of human health, fishing industries and tourism. Unreliable prediction of the potential risk (toxicity) of a bloom can lead to unnecessary closures of fisheries and have severe economic impacts. Since the toxicity of harmful blooms can vary, based on environmental factors, current monitoring of the presence of a HAB species is limited as a measure to predict toxicity. Improved monitoring technologies, for better forecasting of blooms and prediction of their metabolic status and toxicity, could therefore lead to more effective management policies. Given the potential of this research to advance understanding of factors controlling algal bloom formation (and toxicity), the proposed research holds promise to inform marine policy, and several governmental environment departments in particular: Environment Agency, Centre for Environment Fisheries and Aquaculture Science (CEFAS), Joint Nature Conservation Committee (JNCC), Scottish Environmental Protection Agency, European Environment Agency. This could improve protection of shellfish and fishery industries from unnecessary closures which can lead to considerable preventable financial losses. Minimisation of health risks (amnesic shellfish poisoning) associated with human consumption of shellfish contaminated with DA would also benefit consumers. Improved algal bloom management strategies could also minimise negative impacts of algal blooms on tourism and recreational industries such as water sports that rely on a healthy marine environment.

Biotechnology and Industry:

There is enormous interest in the discovery of novel bioactive compounds (such as growth promoting/antimicrobial compounds), for biotechnology. The focus of this proposal on largely unexplored mechanisms of signalling between marine microbes holds promise to identify novel anti-microbial/growth-promoting compounds that could be of use as nutraceuticals. Moreover, algae have attracted attention globally as a potential feedstock for a bio-based economy. Through providing basic insight into algal physiology, ecology, and biochemistry, the work proposed will increase our expertise in algal cultivation and exploitation for industrial purposes.

Medicine and Pharmaceuticals:

Microbial ion channels have made invaluable contributions to advances in understanding in animal biology and human disease, as models for studying ion channel function. The simplified structure of bacterial sodium channels (Navbacs), for instance, opened the door to structural and functional studies of sodium channels and has contributed to drug discovery efforts over the past decade or so. My proposed research - that has potential to identify and characterise novel eukaryote ion channels - has promise to identify new models to study ion channel structure and function, and thus potential to impact animal-related fields including pharmacology, physiology and drug discovery.

Given the likely influences on broad academic disciplines (outlined in academic beneficiaries) I anticipate to publish in high visibility multidisciplinary journals, contributing to maintaining the UK's reputation for scientific excellence.