Award details

Unravelling the neuroendocrine signalling pathways guiding the developmental transition of marine invertebrate larval settlement

Reference	BB/T00990X/1
Principal Investigator / Supervisor	Dr Elizabeth Williams
Co-Investigators / Co-Supervisors
Institution	University of Exeter
Department	Biosciences
Funding type	Research
Value (£)	1,001,662
Status	Current
Type	Fellowships
Start date	04/05/2020
End date	03/05/2025
Duration	60 months

Abstract

For many marine invertebrates, larval settlement is a key developmental transition. This process is strongly linked to the environment in that larvae must detect specific cues to determine the time and place of settlement. How environmental cues are detected and activate internal hormone signalling to regulate larval settlement is not yet clear. To better understand this, I will investigate larval settlement in the polychaete Platynereis dumerilii. Platynereis settlement is internally regulated by myoinhibitory peptide (MIP) signalling through two different receptors, a MIP-activated G protein-coupled receptor (MAG) and a MIP-gated ion channel (MGIC). My recent identification of diatom biofilms as a cue for Platynereis larval settlement provides an opportunity to test the link between external and internal settlement signals in a system amenable to detailed molecular analyses. Here, I will characterize the response of Platynereis larvae to different diatoms. Using calcium imaging and transcriptome analyses, I will investigate short- and long-term responses of larvae to diatom cues. Through phenotypic characterization of MIP- and MIP receptor-knockout lines, I will dissect the contribution of MIP signalling to settlement and assess its link to environmental cue detection. I will also investigate whether thyroid hormone signalling is downstream of MIP signalling during Platynereis larval settlement. To determine whether the function of MIP in larval settlement is conserved throughout protostomes, I will use synthetic MIP treatments to characterize MIP function in three invertebrate species; the oyster Crassostrea gigas, the mussel Mytilus edulis, and the prawn Litopenaeus vannamei. Understanding how external and internal signals combine to guide the developmental transition of marine invertebrate settlement will inform our understanding of animal-microalgae interactions and the evolution of environmentally-guided animal development.

Summary

Many marine invertebrates have a life cycle with a free-swimming larva that spends time in the plankton before settling to the sea floor. Here, the larva undergoes metamorphosis to its adult form. Larval settlement and metamorphosis is an excellent example of the important role that environment can play during animal development, since for many larvae, this process is initiated by specific environmental cues. While the regulation of insect, frog and fish metamorphosis is well known, metamorphosis occurs in at least 15 other animal groups. To fully understand how the environment regulates development, we need to investigate the external cues and internal neuroendocrine signalling that guide metamorphosis beyond insects and vertebrates, and in different environments. Currently we lack a complete understanding of the settlement process, from environmental cue to internal signalling, in any marine invertebrate. In my research at the University of Exeter, I will explore how larvae detect specific environmental cues which activate internal neuroendocrine signalling. I will use the marine worm, Platynereis dumerilii, as my main research organism due to its ease of culture in the lab, the availability of molecular tools and resources in this species, and the wealth of prior knowledge regarding its larval settlement that I can build on. Previous data shows that Platynereis are induced to settle by microalgae known as diatoms, and that a neuronal signalling molecule known as myoinhibitory peptide (MIP) regulates larval settlement behaviour. My research project has four main aims: 1. Characterize the response of Platynereis larvae to diatom cues. In collaboration with Dr Glen Wheeler and Dr Katherine Helliwell at the Marine Biological Association, Plymouth, I will test the response of Platynereis larvae to a variety of diatom species and extracts. I will also measure the neuronal activity of individual larvae exposed to diatoms to identify the larval cells responsible for detecting these cues. Aim 2. Determine whether MIP is linked to the detection of diatom cues. Using recent advances in genome editing technology, I will generate mutant Platynereis larvae that lack either MIP, or one of its two receptors. I will measure the response of mutant larvae to diatoms to test the hypothesis that if MIP signalling is directly activated by diatoms, then mutant larvae will not respond to the diatoms. Aim 3. Determine if MIP induces larval settlement in other marine invertebrates. In collaboration with Dr Rob Ellis at the University of Exeter, I will test whether synthetic MIP treatment induces larval settlement and metamorphosis in a prawn, mussel and oyster species used in local aquaculture. This will establish whether the function of MIP was conserved during the evolution of different marine invertebrates. Aim 4. Identify the downstream neuroendocrine signalling regulated by MIP to control Platynereis larval settlement. Using largescale sequencing of expressed genes, I will identify genes that are activated or repressed by MIP signalling and diatom exposure, providing insight into the physiological changes occurring at settlement. Thyroid hormone has long been suspected to play a role in marine invertebrate larval settlement. In collaboration with Professor Vincent Laudet at the Oceanological Institute of Banyuls-sur-mer, France, I will measure changes in thyroid hormone levels during larval settlement to investigate whether it is a regulator of settlement. Understanding of the importance of different microhabitats as inducers of larval settlement, and identifying downstream hormonal signalling pathways, can be exploited to induce or deter larval settlement. This knowledge has the potential to provide insights into improving invertebrate aquaculture productivity and developing novel antifouling strategies. Project findings may also assist in the repopulation of declining natural marine habitats with key invertebrates.

Impact Summary

Understanding how external cues link to myoinhibitory peptide (MIP) signalling during Platynereis larval settlement will increase our understanding of how the environment and neuroendocrine system combine to regulate the timing of developmental transitions in the sea. The question of how and why marine invertebrate larvae settle where they do is relevant to several challenges in today's marine environment. The primary industry that stands to benefit from my proposed research is the aquaculture industry, the world's fastest growing food production sector. In aquaculture facilities, especially shellfish and crustacean aquaculture, the larval-juvenile transition is a major production bottleneck. Methods for the efficient and timely induction of larval settlement, for example, through exploitation of the MIP signalling pathway, would lead to increased productivity and growth. In addition to polychaetes, both molluscs and crustaceans also express the MIP neuropeptide, and I am determined to investigate MIP function in these phyla. A more precise understanding of how and why larvae choose specific settlement sites can also assist the development of effective antifouling strategies. Biofouling by marine invertebrates is a major problem in the aquaculture and shipping industries, costing millions annually. Current antifouling methods can be costly, time consuming and harmful to the environment. My proposed research has the potential to identify new molecular targets for the development of novel antifouling technologies preventing the sensory detection of cues for larval settlement. Polychaete aquaculture has expanded in recent years as the importance of these worms not only as highly efficient bait, but also as an indispensable food supplement for fish and crustaceans, is increasingly recognized. Polychaetes of the Nereididae family, which includes Platynereis, contain high levels of proteins and omega-3 fatty acids essential for broodstock diets. Polychaetes can convert land-based aquaculture-generated waste to a highly nutritional food source for other aquaculture species, leading to the development of polyculture systems that enhance aquaculture sustainability, reduce environmental impact, and increase industry profits. A key focus area for the expansion of polychaete culture is the development of rearing techniques and grow-out procedures that will allow the culture of new species. The ecotoxicology industry also stands to benefit from this research. Platynereis is an ecologically relevant species with high potential for use in marine ecotoxicology studies. Elucidating the neuroendocrine signalling pathways of Platynereis larvae will facilitate the use of Platynereis as a model for studying the environmental impacts of endocrine disruptors. Increased knowledge of the natural cues for and molecular mechanisms underlying larval settlement may also be used to promote survival and growth during the metamorphic transition in natural marine invertebrate populations. Knowledge of larval behaviour and settlement preferences is of interest to environmental policy-makers as it can improve the planning and selection of sites for marine reserves. In the face of rapid climate change and increased frequency of coral reef bleaching, this knowledge can also contribute to attempts to repopulate benthic marine habitats with key invertebrate species. This information is also of interest to the third sector, specifically organizations dedicated to marine conservation. Due to its impact on aquaculture, fishing, biofouling and marine conservation, knowledge of marine invertebrate larval settlement also stands to benefit the general public. Increased public awareness of the widespread presence of larval settlement and metamorphosis and the importance of this developmental transition to the success of diverse species will foster enthusiasm for and a broader understanding of life cycle evolution and natural history.

Committee	Research Committee A (Animal disease, health and welfare)
Research Topics	X – not assigned to a current Research Topic
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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