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The Biotechnological Value of a Novel Potent Marine Biotoxin from the Polychaete Worm Eulalia Viridis: Chemical and Toxicological Evaluation

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The Biotechnological Value of a Novel Potent Marine Biotoxin from the Polychaete Worm Eulalia Viridis: Chemical and Toxicological Evaluation Ana Patrícia Carreira Rodrigo Mestre em Engenharia do Ambiente The biotechnological value of a novel potent marine biotoxin from the polychaete worm Eulalia viridis: chemical and toxicological evaluation Dissertação para obtenção do Grau de Doutor em Ambiente e Sustentabilidade Orientador: Prof. Doutor Pedro Manuel Broa Costa, Professor Auxiliar, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Co-orientador: Prof. Doutora Maria Alexandra Núncio de Carvalho Ramos Fernandes, Professora Auxiliar, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Prof. Doutora Maria Helena Costa, Professora Catedrática, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Júri: Presidente: Prof. Doutora Maria Paula Antunes Arguente(s): Prof. Doutora Maria Leonor Quintais Cancela da Fonseca Prof. Doutor Henrique Manuel Roque Nogueira Cabral Prof. Doutor Manu Soto Prof. Doutor Pedro Manuel Brôa Costa Novembro de 2020 Ana Patrícia Carreira Rodrigo Mestre em Engenharia do Ambiente The biotechnological value of a novel potent marine biotoxin from the polychaete worm Eulalia viridis: chemical and toxicological evaluation Dissertação para obtenção do Grau de Doutor em Ambiente e Sustentabilidade Orientador: Prof. Doutor Pedro Manuel Broa Costa, Professor Auxiliar, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Co-orientador: Prof. Doutora Maria Alexandra Núncio de Carvalho Ramos Fernandes, Professora Auxiliar, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Prof. Doutora Maria Helena Costa, Professora Catedrática, Faculdade de Ciências e Tecnologia da Universidade Nova de Lisboa Júri: Presidente: Prof. Doutora Maria Paula Antunes Arguente(s): Prof. Doutora Maria Leonor Quintais Cancela da Fonseca Prof. Doutor Henrique Manuel Roque Nogueira Cabral Prof. Doutor Manu Soto Prof. Doutor Pedro Manuel Brôa Costa Novembro de 2020 COPYRIGHT Autorizo os direitos de copyright da minha tese de doutoramento, com o título: "The biotechnological value of a novel potent marine biotoxin from the polychaete worm Eulalia viridis: chemical and toxicological evaluation" A Faculdade de Ciências e Tecnologia e a Universidade Nova de Lisboa tem o direito, perpétuo e sem limites geográficos, de arquivar e publicar esta dissertação através de exemplares impressos reproduzidos em papel ou de forma digital, ou por qualquer outro meio conhecido ou que venha a ser inventado, e de a divulgar através de repositórios científicos e de admitir a sua cópia e distribuição com objetivos educacionais ou de investigação, não comerciais, desde que seja dado crédito ao autor e editor. iii iv ACKNOWLEDGEMENTS “Do what you love and you will never have to work a day in your life” Even though this is true, if you are not surrounded by great people, what you love would not be sufficient. As such, I would like to start with a special thank you to all my friends from Seatox Lab and specially Pedro, for helping and accompanying me through all the journey. To Cátia and Carla for accompanying me for more than 10 years in all the parties, late night school papers and all the hard work in the laboratory. To Carolina and Diana M. for the scientific motivation and the company in all the lunches and fun dinners. To Mariaelena for the laughs, the motivation and all the ecological and sustainable insight. To Nagore, for the ecological insight and the company during the beach life. To Diana R., despite not being part of the group, is part of the family. Also, a special thank you to all the bachelor and master students that passed through the lab that brought a fresh environment to the lab. Despite small, the Seatox team was essential to walk the walk, from sampling and laboratory work, to keeping the sugar levels up with all the pastry that able me to relax and keep working even more motivated. Also, for believing in me even in situations where I don´t and to always keep the best work environment that someone could have. A thank you to my supervisor Alexandra and to the Human Genetics and Cancer Therapeutics lab for all the supervision, warm welcoming into their group and help in the most challenging part of my PhD. A thank you to Pedro Baptista and the whole group for giving me all the technical support and overall picture whenever needed. To Cynthia and Bruno, for making a second workplace, a second home. Also, a thank you to Ana Rita and the Computational Multi-Omics Lab for all the precious help in transcriptomics, for making all the lunches a fun part of the day and extending it to the coffee breaks. To all my friends that accompanied me and hear whenever necessary and help me to stress down and relativize the work during the much-needed breaks in all the extra-activities. To Dulce, Sara and Andreia for all the craziness since primary school and helping me to became who I am. To Rita F. and Tânia for the great times since high school. To Rita, Teresa, Marta and Lopes for the company in all the marathons. To Hugo for the best working buddy in all the cafes and late nights. To Poggi, Tiago, Pedro A., Bruno, Durães and the aforementioned for all the waves shared. To Ana, Papa, David, Igna, Edgar, Macau, Rita, Sofia, Rasta, Katha, Mário and Teresa for being the best climbing buddies, to motivate science discussions and relaxation in the best spots. v To my parents for dealing with the hard times and celebrate the good ones and to always keep interest and proud in my work and life. To my sister for hearing me daily and always be close even living far away. To my nephew, grandpa, aunts, uncles and cousins for always remembering that the basis of life is family and family leads to happiness. And finally to Fred, for all the fresh meals, hugs, always having my back and accompany me in every situation, even when not fully understanding them. vi RESUMO O oceano contém muitos organismos por explorar com características adaptativas que os permitem prosperar no seu meio ambiente. Eulalia viridis é um desses organismos. Esta poliqueta verde clara é predador do intertidal rochoso sem mandibulas, equipado dum muco tóxico, permitindo assim predar invertebrados maiores extraindo pedaços de tecido através da sucção. Motivado pelo valor das toxinas como substâncias bioreactivas e pela ambição da UE de conduzir a Estratégia para o Crescimento Azul, à qual a vasta ZEE portuguesa oferece grandes perspetivas, o potencial biotecnológico desta espécie foi analisado. A análise microanatómica desta minhoca revelou adaptações cruciais na alimentação: existência de papilas sensoriais e células responsáveis pela secreção de muco e toxinas. A sequenciação completa do transcritoma e ensaios toxicológicos revelaram um complexo padrão de toxinas proteicas e enzimas com diversas funções: permeabilização de tecidos, anti-coagulação e bloqueio da atividade neuromuscular. As principais neurotoxinas da Eulalia, “filotoxinas”, são proteínas ricas em cisteínas, que atuam como agentes imobilizadores em mexilhões e outros invertebrados, que são administradas por contacto através do muco. Por sua vez, uma maior toxicidade para com a linha celular do cancro do ovário (A2780) do que células normais, demonstraram propriedades citotóxicas e citoestáticas através da paragem do ciclo celular e indução de morte celular programada pela via extrínseca. As proteínas responsáveis por estes efeitos foram identificadas, através de transcritómica e proteómica. As secreções mucosas da minhoca contêm também complexos proteicos internalizáveis que apresentam fluorescência, cuja emissão é reversivelmente regulada pelo estado redox. Resumindo, as características encontradas nas secreções de uma espécie demonstram o vasto potencial biotecnológico de anelídeos marinhos, como uma fonte valiosa de bioreactivos, mesmo em águas temperadas. O percurso metodológico utilizado, a combinação da ecologia, toxicologia e biologia molecular, permitiu contornar dificuldades da bioprospecção marinha, revelando ser um importante contributo para exploração sustentável de novos biorecursos marinhos. Palavras-chave: Economia Azul; Ensaios in vitro; Muco; Filotoxinas; Proteómica; Transcritómica. vii viii ABSTRACT The ocean’s vastness holds still many unexplored organisms with unique adaptive features that enable them to thrive in their environment. Eulalia viridis is one of them. This uncanny bright green worm is a predatory marine Polychaeta of the rocky intertidal that lacks jaws, but it is equipped with a toxin-containing mucus that enables predating larger invertebrates from which soft tissue is extracted through suction. Motivated by the high-value of toxins as bioreactives and by the European Union’s ambitions of leading the Blue Growth Strategy, for which Portugal’s vast EEZ offers high perspectives; a case-study to explore the biotechnological potential of this species was undertaken. The worm’s microanatomy revealed key adaptations for feeding such as special sensorial papillae and cells responsible for the secretion of mucus and toxins. Whole-transcriptome sequencing and toxicity assays yielded a complex pattern of proteinaceous toxins and enzymes with several functions: tissue permeabilization, coagulation impairment and blocking of neuromuscular activity. The main neurotoxins, “phyllotoxins”, found to be cysteine-rich proteins, act as immobilising agents against mussels and other invertebrate prey and are delivered by contact with mucus. In turn, higher toxicity towards ovarian cancer cell line (A2780) than normal cells, involved cytotoxic and cytostatic properties through cell cycle arrest
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