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Marine Biofilms: Targets of Cyanobacterial

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Marine Biofilms: Targets of Cyanobacterial Marine biofilms: targets of cyanobacterial compounds towards a natural D antifouling strategy Jorge Tiago Vieira Ferreirinha Antunes Doutoramento em Biologia Departamento de Biologia Ano de 2019 Orientador Doutor Pedro Leão, CIIMAR Coorientador Prof. Doutor Vitor Vasconcelos, FCUP and CIIMAR ii Marine biofilms: targets of cyanobacterial bioactive compounds towards a natural antifouling strategy SFRH/BD/99003/2013 Jorge Tiago Vieira Ferreirinha Antunes Blue Biotechnology and Ecotoxicology (BBE) and Cyano Natural Products (CNP) research teams Interdisciplinary Centre of Marine and Environmental Research (CIIMAR) Supervisor: Pedro Leão, CIIMAR Co-supervisor: Professor Vítor Vasconcelos, FCUP and CIIMAR Faculty of Sciences of University of Porto, 2019 iii Jorge Antunes acknowledges a PhD scholarship SFRH/BD/99003/2013 from FCT (Fundação para a Ciência e Tecnologia). This work was supported by FCT - Foundation for Science and Technology - under project UID/Multi/04423/2013 and by the Structured Program of R&D&I INNOVMAR - Innovation and Sustainability in the Management and Exploitation of Marine Resources (reference NORTE-01-0145-FEDER-000035, Research Line NOVELMAR), which was funded by the Northern Regional Operational Programme (NORTE2020) through the European Regional Development Fund (ERDF) and by the project CVMAR+I (0302_CVMAR_I_1_P) funded by the program Interreg V Portugal-Spain (POCTEP) through the ERDF. Funding was also provided by the project NASCEM PTDC/BTA-BTA/31422/2017 (POCI- 01-0145-FEDER-031422), financed by the FCT, COMPETE2020 and PORTUGAL2020. iv Personal acknowledgements Writing this dissertation was, for me, one of the most challenging tasks I ever endeavored, one I would surely fail if not for the help of a number of wonderful people I was lucky enough to meet. In particular, I would like to sincerely thank my supervisor, Doutor Pedro Leão, the best guide I could ever hope for his insightful, good humor– and always illuminating – commentaries. I also thank him for his constant thoroughness and constant readiness to help. His willingness to give me enough scientific independence during this project of discovery, and to challenge me for always strive for the best, surely allowed me to grow as a researcher and as a scientist. I would like also to heartily thank my co-supervisor, Professor Doutor Vitor Vasconcelos for accepting my proposal to conduct this thesis in a such an interesting topic, and for welcoming me again in such a dynamic, good-spirited and exceptional team. His helpfulness, generosity and scientific knowledge along these last years, made me joyful to work in such an outstanding institution such as CIIMAR. I also thank all my colleagues particularly in the BBE and CNP teams, as well in other CIIMAR teams for all their support, and friendship who are unfortunately too many to mention all by name. I would like to mention, however some who helped me more directly both in the lab, as well in fruitful scientific discussions, and who helped me to carry on through this difficult process until the end. Therefore, a special mention to Anoop, Aldo, António, Tito, Cidália, Adriana and Teresa. An even more special mention to Joana, my closest teammate during these last years, for her friendship and help during our marine fouling scientific projects, the best colleague I could hope for. Finally, I would like to thank my family for their unconditional support and patience, particularly my parents for their understanding and love, to whom I dedicate this thesis, and who are the true biologists. v Abstract Marine biofouling remains an unresolved problem with serious economic impact for different industries. Marine biofilms are the initial step of the marine fouling process in artificial surfaces and are the preferential substrata for the settlement of macroinvertebrate larvae and macroalgae spores. In this thesis, an extensive and critical literature review was carried out to digest current information on the distribution of marine biofilms, the already known chemical cues involved in their formation, as well the overall importance of marine biofilms for the marine fouling process. In addition, to understand how the marine biofilm formation process evolves, we employed amplicon-based NGS (Next-generation sequencing) methodologies to characterize early-stage marine biofilms growing on steel surfaces in two distinct seasons in the port of Leixões in Northern Portugal. The 16S rRNA gene sequencing data analysis demonstrated distinct taxonomic and functional profiles of the marine biofilm communities in the sampled seasons, suggesting that seasonality is a major factor influencing the diversity of those prokaryotic communities. Furthermore, the sampled biofilms revealed the presence of pathogenic taxa which, accordingly to our knowledge was not reported previously, and whose abundance was significantly influenced by temporal variations. This knowledge should be important for future anti-fouling and anti-corrosion purposes. After years of application of toxic antifoulants to control biofouling, there is a strong necessity for the development of environmentally friendly antifouling products, and cyanobacteria are a particularly encouraging source of new natural antifouling compounds. An extensive screening was therefore performed with crude organic extracts of 61 cyanobacterial strains of the LEGE Culture Collection (LEGE CC) to test their anti-fouling potential. The obtained fractions of several cyanobacterial strains revealed significant activity against the growth of microfouling organisms involved in marine biofilm formation (bacteria and diatoms) and inhibited the quorum-sensing (QS) phenomenon, which is associated with biofilm formation. Subsequent work resulted in a set of HPLC-PDA purified bioactive fractions from a marine cyanobacterial strain whose structure is being elucidated by spectroscopic methods. vi Additionally, the already known cyanobacterial compounds portoamides, isolated from a marine cyanobacterium from the LEGE CC, were also tested for their antifouling potential. A multi-bioassay approach revealed a wide spectrum antimicrofouling, anti- macroinvertebrate settlement, and anti-biofilm activity of those compounds, while displaying no toxicity to target and non-target organisms, suggesting that portoamides have a potential to be used as new environmentally friendly antifouling agents. We have also optimized an anti-biofilm assay protocol that should be of interest for the discovery of bioactive compounds with anti- marine biofilm activity which is indispensable for the discovery of efficient broad-spectrum antifouling compounds. Keywords: anti-biofilm; antifouling; bioactive compounds; cyanobacteria compounds; marine biofilms; marine biofouling; next-generation-sequencing; quorum-sensing. vii Resumo As camadas incrustantes causadas por organismos marinhos são um problema com grandes consequências económicas para diferentes indústrias. Os biofilmes marinhos são o primeiro passo no processo de colonização das camadas incrustantes em superfícies artificiais, e constituem superfícies preferenciais para a colonização e adesão de larvas de macroinvertebrados, e de esporos de macrogalgas. Neste projeto de doutoramento, um artigo de revisão foi escrito para discutir a distribuição de biofilmes marinhos, os compostos químicos envolvidos na sua formação, assim como a importância dos biofilmes no contexto das camadas incrustantes marinhas. A tecnologia de sequenciação de nova geração foi adotada para caracterizar os biofilmes marinhos que cresceram em superfícies de metal em duas estações distintas do ano no porto de Leixões, no Norte de Portugal. A análise dos dados de sequenciação de 16S RNA demonstrou um perfil taxonómico e funcional distinto nas duas estações do ano, sugerindo que o tempo e a estação do ano influenciam fortemente a composição taxonómica e funcional desses biofilmes. Adicionalmente, foram identificados nesses biofilmes grupos taxonómicos associados a situações patogénicas que, segundo o nosso conhecimento, não tinham sido descritos em estudos anteriores sobre biofilmes marinhos e cuja abundância foi significativamente influenciada pelas variações temporais testadas. Esta informação pode ter relevância para futuras estratégias eficientes de controlo de crescimento de camadas incrustantes e de biofilmes marinhos. Depois de anos de aplicação de produtos anti-incrustante tóxicos, existe uma grande necessidade do desenvolvimento de produtos que não sejam danosos para o ambiente, e as cianobactérias são uma fonte particularmente relevante para a descoberta de novos compostos naturais devido ao potencial bioativo dos seus metabolitos secundários. Neste projeto de doutoramento, um rastreio abrangente foi efetuado com os crudes de 61 estirpes de cianobactérias da coleção de culturas do LEGE (LEGE CC) para identificar o seu potencial anti-incrustante. Várias estirpes demonstraram uma significativa bioatividade contra bactérias marinhas e diatomáceas, e viii inibiram igualmente o fenómeno de percepção de quórum (quorum-sensing). Trabalho posterior levou à obtenção de uma fração bioativa purificada por HPLC-PDA, cuja estrutura será elucidada por métodos de espectrometria de massa de alta resolução. Adicionalmente, os já conhecidos compostos de cianobactérias, portoamidas, isolados de uma cianobactéria pertencente à LEGE CC, também foram testados contras os mesmo painéis de organismos. Uma série de ensaios distintos revelou uma abrangente atividade destes compostos, assim como uma significativa
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