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In the Hemiascomycetes Yeasts Biotechnology Evolution and Bioinformatics Analysis of the Drug: H+ Antiporter Family 1 (DHA1) in the hemiascomycetes yeasts André Miguel Moreira Machado Thesis to obtain the Master of Science Degree in Biotechnology Supervisors: Prof. Dr. Isabel Maria de Sá Correia Leite de Almeida Dr. Paulo Jorge Moura Pinto da Costa Dias Examination Committee Chairperson: Prof. Dr. Arsénio do Carmo Sales Mendes Fialho Supervisor: Dr. Paulo Jorge Moura Pinto da Costa Dias Members of the Committee: Dr. Margarida Isabel Rosa Bento Palma July 2016 Agradecimentos Primeiramente gostaria de agradecer à minha orientadora Professor Isabel Sá-Correia por me dar a oportunidade de participar do Grupo de Ciências Grupo de Pesquisa Biológica (BSRG), por me agilizar o máximo possível os processos burocráticos na entrega desta dissertação e por ter paciência para alunos como eu. Por outro lado, gostaria de fazer também aqui um especial agradecimento ao meu orientador Dr. Paulo Dias, que me guiou ao longo deste trabalho, durante o último ano e meio, e me ajudou em todas as fases da sua realização de forma incansável, desde o desenvolvimento de metodologias até á escrita e elaboração do documento. Devo ainda salientar que sem a sua exigência e perseverança muito provavelmente não teria adquirido a enorme quantidade de conhecimentos adquiri, a nível informático, biológico e evolutivo. O meu trabalho bioinformático foi realizado dentro grupo BSRG, uma unidade do Instituto de Bioengenharia e Biociências (IBB) que pertence ao Instituto Superior Técnico (IST) e agregado á Universidade de Lisboa. A este grupo gostaria de agradecer todo suporte técnico que me deram e todo o bom ambiente que proporcionaram. Passando para os agradecimentos mais pessoais e personalizados, antes de mais, é importante referir que gostaria de poder ter presente, na minha vida, todas as pessoas que me ajudaram ao longo desta fase da minha vida académica. No entanto isso não é possível. Isto fez-me refletir sobre todas as prioridades que devemos ter durante a nossa existência, e todo o valor que devemos dar a quem mais nos apoia. Aos meus Avós paternos, que faleceram ambos durante o decorrer deste Mestrado e que sempre me deram um apoio incondicional e irrepreensível, gostaria de dedicar todo o trabalho árduo e força de vontade avassaladora que a realização do mestrado e desta tese envolveu. Em respeito a eles e porque a minha língua materna é a portuguesa, escrevo estes agradecimentos em português. Gostaria de agradecer também aos meus Pais, e Irmão, pelas palavras de ânimo e carinho que me fizeram vencer todos os obstáculos, pelas condições favoráveis que me proporcionaram e tornaram possível o vencer de mais uma batalha. Uma parte deste trabalho é, sem dúvida, uma conquista desta minha especial família. Gostaria ainda de agradecer aos meus fiéis amigos Filipe Tente, João Nuno, Pedro Parente, João Pereira que apesar de algumas vezes afastados, muitas vezes foram os mais próximos. Ao meu grande amigo Gonçalo Curveira Santos a oportunidade que me deu de viver com ele em Lisboa, e por todo o apoio, tanto a nível pessoal como profissional. Gonçalo tu vais ser uma das mentes brilhantes deste país, continua a lutar. Aos meus amigos do IST, um especial agradecimento ao Carlos Branco, Pedro Santos, Miguel Gomes, Simion Petru e Rafael Crisóstomo entre outros (sabem quem são) por toda a ajuda informática, amizade e momentos de lazer que me fizeram manter a sanidade mental (ou não). Por fim, e porque o melhor vem sempre no final, quero agradecer á minha companheira de vida Ana Ferreira, por todo apoio científico/pessoal, incentivo extraordinário, e alegrias constantes que garantiram e vão garantir sempre que eu dê o melhor de mim apesar do cansaço e dos dias mais difíceis. Esta tese é tanto minha quanto tua. I Abstract The Saccharomyces cerevisiae 12-spanner drug: H+ antiporters (DHA1) and 14- spanner drug: H+ antiporters (DHA2) of the Major Facilitator Superfamily (MFS) are involved in Multidrug/Multixenobiotic resistance (MDR/MXR) phenomenon. The aim of the present work is to reconstruct and characterize the evolution of the DHA1 genes encoded in 33 hemiascomycetes strains classified in the Saccharomycetaceae taxonomic family, (corresponding to a total of 29 yeast species). The DHA1 and DAG (DHA2, ARN, GEX) proteins encoded in the genomes of 61 additional strains, spanning more than 15 hemiascomycetous taxonomic families, were also identified and briefly analysed. The constraining and traversing of a network representing the blastp pairwise similarity relationships established between more than one million hemiascomycetous translated ORFs allowed the identification of 1382 bona fide full-size DHA1 transporters (after correction of problematic translated ORFs). The evolutionary history of the DHA1 genes encoded in the genome sequences of 33 Saccharomycetaceae strains was reconstructed by combining phylogenetic and gene neighbourhood approaches. Twenty-six DHA1 phylogenetic clusters were identified and nine DHA1 gene lineages reported in previous published studies were revised and extended. State-of-the-art methodologies on phylogeny, comparative genomics and protein evolution were used to advance the existing knowledge on the still poorly biochemically characterized DHA1 transporters, allowing obtaining new insights on how the functional diversification of these proteins is related with ancestral genomic events, such as the Whole Genome Duplication (WGD), local gene duplications and losses, Horizontal Gene Transfers (HGT) between yeast species, chromosomal rearrangements, and other genome reshaping phenomena. Keywords: DHA1, DAG, Saccharomyces cerevisiae, Multidrug resistance, Saccharomycetaceae, Whole Genome Duplication. II Resumo Os genes do organismo Saccharomyces cerevisiae, da família 1(DHA1) e família 2(DHA2) de antiportadores de drogas, e da superfamília de facilitadores, estão envolvidos na resistência a múltiplas drogas/xenobióticos. O objetivo deste trabalho foi reconstruir e caracterizar a evolução dos genes DHA1, codificados no genoma de 33 estirpes de Hemiascomycetos classificadas na família taxonómica Saccharomycetaceae (correspondendo ao total de 29 espécies). Paralelamente, foram identificadas e analisadas, de forma breve, as proteínas DHA1 e DAG codificadas no genoma de 61 estirpes adicionais que estão classificadas em mais de 15 famílias de Hemiascomycetos. A constrição e atravessamento de uma rede de similaridade de pares blastp entre mais de um milhão de ORF’s em Hemiascomycetos, permitiu identificar 1382 transportadores DHA1 não fragmentados (após a correção das ORF’s problemáticas). Assim, foi reconstruída a historia evolutiva dos genes DHA1, codificados no genoma das 33 estirpes Saccharomycetaceae, com recurso á combinação de técnicas de filogenia e de vizinhança de genes. Isto permitiu identificar 26 grupos filogenéticos de genes DHA1, e fazer uma revisão e ampliação de 9 linhagens de genes DHA1 publicadas em estudos anteriores. As metodologias do estado de arte sobre filogenia, genómica comparativa, evolução proteica foram utilizadas para expandir o conhecimento acerca destes transportadores DHA1, ainda pouco caracterizados bioquimicamente, permitindo obter novas conclusões sobre o envolvimento da diversificação funcional destas proteínas com os eventos genómicos ancestrais , da duplicação total do genoma ,duplicações locais e perdas de genes, transferências horizontais de genes entre espécies de leveduras, rearranjos cromossômicos, e outros fenômenos de remodelação genómica. Palavras-chave: DHA1, DAG, Saccharomyces cerevisiae, Resistência a Múltiplas drogas, Saccharomycetaceae, Duplicação total do genoma. III Contents Agradecimentos ........................................................................................................................................ I Abstract.................................................................................................................................................... II Resumo .................................................................................................................................................. III List of figures .......................................................................................................................................... IV List of tables .......................................................................................................................................... VII List of abbreviations .............................................................................................................................. VIII 1. Goals and brief introduction to the thesis study ............................................................................... 1 2. General Introduction ......................................................................................................................... 3 2.1. Yeasts: Biotechnology, taxonomy and diversity ...................................................................... 3 2.1.1. Biotechnology and applications ....................................................................................... 3 2.1.2. Evolution, taxonomy and diversity of yeasts ................................................................... 5 2.2. Yeasts: Comparative genomic, and evolution ....................................................................... 11 2.2.1. Comparative genomics .................................................................................................. 11 2.2.2. Comparative genomics and evolution of
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