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Marine Fungal Community Associated with Standing Plants of Spartina Maritima (Curtis) Fernald

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Marine Fungal Community Associated with Standing Plants of Spartina Maritima (Curtis) Fernald UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS Marine fungal community associated with standing plants of Spartina maritima (Curtis) Fernald Doutoramento em Biologia Especialidade em Microbiologia Maria da Luz Jeremias Cardinha do Maio Calado Tese orientada por: Prof. Doutora Margarida Barata e Prof. Doutor Ka-Lai Pang Documento especialmente elaborado para a obtenção do grau de doutor 2016 UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS Marine fungal community associated with standing plants of Spartina maritima (Curtis) Fernald Doutoramento em Biologia Especialidade em Microbiologia Maria da Luz Jeremias Cardinha do Maio Calado Tese orientada por: Prof. Doutora Margarida Barata e Prof. Doutor Ka-Lai Pang Júri: Presidente: ● Doutor José Simões Vogais: ● Doutor Nelson Lima ● Doutora Raquel Coelho ● Doutor Alan Phillips ● Doutor José Paulo Sampaio ● Doutora Maria Isabel Caçador ● Doutora Margarida Barata Documento especialmente elaborado para a obtenção do grau de doutor Fundação para a Ciência e Tecnologia (FCT) 2016 Tese apresentada à Universidade de Lisboa para obtenção do grau de Doutor em Biologia, especialidade em Microbiologia O trabalho de investigação apresentado nesta tese foi apoiado financeiramente pela Fundação para a Ciência e Tecnologia pela atribuição da Bolsa de doutoramento com a referência SFRH/BD/48525/2008 A tese deve ser citada como: Calado ML (2016) Marine fungal community associated with standing plants of Spartina maritima (Curtis) Fernald. Ph.D. Thesis, Faculty of Sciences of University of Lisbon Thesis presented at University of Lisbon for obtaining doctoral degree in Biology, Microbiology The research work presented in this thesis was supported financially by Foundation for Science and Technology (FCT) through a Ph.D. grant with the reference SFRH/BD/48525/2008 This thesis should be cited as: Calado ML (2016) Marine fungal community associated with standing plants of Spartina maritima (Curtis) Fernald. Ph.D. Thesis, Faculty of Sciences of University of Lisbon 3 4 TABLE OF CONTENTS ACKNOWLEDGMENTS 7 RESUMO 9 ABSTRACT 13 LIST OF FIGURES 15 LIST OF TABLES 17 THESIS FRAMEWORK 19 CHAPTER 1 – General Introduction 21 1.1 Marine fungi – a brief review 23 1.2 Salt marsh fungi 31 1.3 Objectives 51 1.4 References 51 CHAPTER 2 - Diversity and ecological characterization of sporulating higher 63 filamentous marine fungi associated with Spartina maritima (Curtis) Fernald in two Portuguese salt marshes CHAPTER 3 - Ecological preferences of marine fungi associated with standing 111 decaying plants of Spartina maritima (Curtis) Fernald CHAPTER 4 – Final overview 159 4.1 General conclusions 161 4.2 Future perspectives 167 4.3 References 167 5 6 ACKNOWLEDGMENTS This thesis represents the end of a long, demanding and challenging, but undoubtedly enriching and rewarding journey. It definitely made me grow professionally and personally. However, the execution and conclusion of this journey would not have been possible without the help and support of several persons, to whom I would like to address my heartfelt gratitude. First of all, I would like to thank my supervisors Professor Margarida Barata and Professor Ka- Lai Pang for kindly receiving me in their labs, giving me all the conditions I needed to develop my research work, and for their constant support, availability, constructive discussions, helpful “brainstormings” and professional guidance throughout the development of this project. Also, I am truly grateful for their generosity, trust and belief in me, friendship and encouraging and motivational words whenever needed. Secondly, I would like to thank to - Luís Carvalho, for his indispensable help in the statistical analysis of data and valuable and constructive suggestions; - Professor Manuela Carolino, for her kindness and support, and Catarina Gouveia, for being a great lab mate during the long time I spent under the microscope; - Rita Severino and Cristina Oliveira for their precious help in the culture experiment; - Professor Cristina Cruz, for accepting me in her work team and laboratory; - Professor Cristina Figueiredo, for her kindly help and expertise in the lyophilisation process; - and all academic and non-academic staff from the Department of Plant Biology that contributed somehow for this work in different ways and time moments. Thirdly, I would like to express my sincere gratitude to my friends - Egídia Azevedo and Sílvia Mendonça, for their friendship and encouragement along this path; - Shine, Yufen, Cha Cha, Su Su, Iris, Alex and all my Taiwanese colleagues and friends, for welcoming me into their lovely and beautiful country, for being (together with Professor Ka-Lai Pang) my surrogate family for 8 months, and for turning the most challenging part of this thesis into one of the most remarkable experiences of my life; - António Miranda, for being a great office mate and friend and for his peculiar sense of humour that turned our lunch moments into stress-release and laughter therapies; - Joana Rosado, for her friendship in the real sense of the word (thank you for being always present!). Finally, I am really grateful to my family, particularly 7 - Sérgio, for his love, constant encouragement, patience and companionship, and for helping me overcoming frustrating time periods of the research life and difficult periods of my personal life (you definitely changed my life…for the best!); - my nephews Rafael and Lucas, who born during this journey, for colouring my life and for making me discover the powerful love, joy, happiness and privilege of being an aunt; - women of my life to whom I dedicate my thesis (this would never have been possible without our strong and powerful bond!): my sister Isa, my aunts Florbela and Inês, my grandmothers Joana (my sweet star, who unfortunately did not have the chance to testify this moment, but was and will always be the pillar of our family) and Constança, and especially my mother (my anchor), for supporting me at every step of this process and during the hardest moments of my and our lives. 8 RESUMO A presente tese pretendeu contribuir para o aumento do conhecimento relativo às comunidades de fungos marinhos superiores que colonizam ecossistemas intertidais temperados, dada a escassez de estudos desenvolvidos neste domínio em geral, e em Portugal em particular. Especificamente pretendeu-se inventariar as espécies fúngicas associadas a uma das macrófitas mais importantes e dominantes dos sapais da costa portuguesa, a Spartina maritima (Curtis) Fernald, e compreender melhor a dinâmica da comunidade e diversos aspectos da ecologia de cada espécie fúngica. O estudo foi desenvolvido em dois sapais (Castro Marim e Ria de Aveiro) com características distintas, no que respeita à localização geográfica, configuração física, estado de conservação e representatividade da planta hospedeira. O sapal de Castro Marim situa-se no troço final do estuário do Guadiana, na costa sudeste de Portugal (37.23° N, 7.42° W), e está incluído numa Reserva Natural; apresenta, por isso, estatutos especiais de protecção e uma comunidade de S. maritima bem conservada, que se distribui paralelamente ao rio numa faixa contínua. O sapal da lagoa costeira da Ria de Aveiro localiza-se na costa noroeste de Portugal (40.62° N, 8.74° W) e integra uma complexa rede de canais sujeita a fortes pressões antrópica; nesta área, a comunidade de S. maritima está muito fragmentada e dispersa ao longo da faixa de vegetação. A amostragem da comunidade de fungos marinhos envolveu a recolha de 195 plantas inteiras, maduras, enraizadas e em posição natural de S. maritima durante 2 anos (de Outubro de 2010 a Agosto de 2012), com uma periodicidade de 2 meses; recolheram-se 20 plantas de cada área de estudo nos primeiros 3 meses, e 15 plantas nos restantes períodos. Em laboratório, cada planta, previamente lavada e seca ao ar, foi separada em nove categorias de substrato, de acordo com as estruturas vegetais que a compunham e estado fisiológico das mesmas; especificamente, em bainhas vivas, bainhas senescentes, bainhas em decomposição, caules vivos, caules senescentes, caules em decomposição, limbos vivos, limbos senescentes e limbos em decomposição. As denominações “vivo”, “senescente” e “em decomposição”, caracterizaram tecidos verdes, amarelos e acastanhados, com estrutura física nada, pouco ou bastante alterada respectivamente. A identificação dos fungos marinhos recorreu a dois métodos distintos, mas complementares; (1) a observação directa de estruturas fúngicas (esporos, estruturas de frutificação e hipopódios) e (2) a sequenciação da região ITS (Internal Transcribed Spacers) do DNA ribossomal nuclear (rDNA). O primeiro método envolveu a análise individual de cada substrato vegetal à lupa; as estruturas fúngicas detectadas nesse substrato foram observadas ao microscópio e identificadas com base nas suas características morfológicas, recorrendo a chaves dicotómicas específicas para identificação de fungos marinhos. Adicionalmente registou-se a distribuição vertical e densidade das estruturas fúngicas de cada espécie. No período de Fevereiro de 2012 a Agosto 9 de 2012, foram ainda recolhidas 5 plantas extras, as quais foram lavadas e imediatamente observadas. Algumas estruturas de frutificação (ascocarpos ou picnídios) diferenciadas neste material vegetal fresco foram extraídas e utilizadas na obtenção de culturas puras, através do método de esporo único. Os fungos isolados foram preservados por três métodos distintos: (1) crescimento activo em Corn Meal Agar (CMA) preparado com água do mar diluída (50%), a 4
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