Signal Molecules in Ctenophores: Quest for the Earliest Transmitters

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Ctenophores, also known as comb-jellies, are marine invertebrates that show an unprecedented capacity for regenerating. Their nervous system has two networks of interconnected cells and an elementary brain, and information travels from one nerve cell to another differently than in any other animal group. This research will reveal how comb-jellies build their nervous systems as compared to those of all other animals, and discover new molecules that control nerve cell communication in comb-jellies. Learning about these enigmatic organisms will open new horizons in scientific knowledge about alternative ways to build nerve cells and neural circuits, and will also decipher ways to rebuild damaged nervous systems. Data from these experiments will be deposited in publically web-accessible servers for the broader scientific community. This work will also provide unique opportunities for field education and training of students and the general public by using mobile marine laboratories and digital resources that are accessible world-wide. Wild-captured animals from the genuses Pleurobrachia and Mnemiopsis are the major experimental models for this research. Neuron-specific, single-cell approaches will be used to study gene expression, metabolomics, proteomics, connectivity and function with the overall goal of identifying novel neurotransmitters and neural specification molecules in cell populations forming the two distinct neural nets (ectodermal vs mesoglea-derived) and aboral organ (the analog of the elementary brain) of diverse ctenophore species. Specific outcomes will be: (1) deciphering a new chemical language in neural systems by genome-scale annotation of neurogenic and myogenic molecular pathways and transcription factors using single-cell RNA-seq and epigenome sequencing technologies; (2) tracing neuronal identities throughout development; (3) identifying and characterizing novel signal molecules or neurotransmitters using capillary electrophoresis and mass spectrometry complemented by physiological approaches; and (4) developing potential models to explain the neural origins and evolutionary diversification of synapses.