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Agrupamentos Gênicos Envolvidos Na UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL CENTRO DE BIOTECNOLOGIA PROGRAMA DE PÓS-GRADUAÇÃO EM BIOLOGIA CELULAR E MOLECULAR AGRUPAMENTOS GÊNICOS ENVOLVIDOS NA BIOSSÍNTESE DE METABÓLITOS SECUNDÁRIOS NO FUNGO ENTOMOPATOGÊNICO Metarhizium anisopliae: IDENTIFICAÇÃO GÊNOMICA E PADRÕES DE EXPRESSÃO EM CUTÍCULAS DO CARRAPATO Rhipicephalus microplus Dissertação de Mestrado Nicolau Sbaraini Oliveira Porto Alegre, Outubro de 2016 UNIVERSIDADE FEDERAL DO RIO GRANDE DO SUL CENTRO DE BIOTECNOLOGIA PROGRAMA DE PÓS-GRADUAÇÃO EM BIOLOGIA CELULAR E MOLECULAR AGRUPAMENTOS GÊNICOS ENVOLVIDOS NA BIOSSÍNTESE DE METABÓLITOS SECUNDÁRIOS NO FUNGO ENTOMOPATOGÊNICO Metarhizium anisopliae: IDENTIFICAÇÃO GÊNOMICA E PADRÕES DE EXPRESSÃO EM CUTÍCULAS DO CARRAPATO Rhipicephalus microplus Dissertação submetida ao Programa de Pós- Graduação em Biologia Celular e Molecular do Centro de Biotecnologia da Universidade Federal do Rio Grande do Sul como requisito parcial para obtenção do Grau de Mestre em Biologia Celular e Molecular. Nicolau Sbaraini Oliveira Orientador: Prof. Dr. Augusto Schrank Co-orientador: Dr. Rafael Lucas Muniz Guedes Porto Alegre, Outubro de 2016 I Este trabalho foi desenvolvido no Laboratório de Biologia Celular e Molecular de Fungos Filamentosos da Universidade Federal do Rio Grande do Sul, com apoio do Rede Avançada em Biologia Computacional (RABICÓ), do Centro Nacional de Desenvolvimento Científico e Tecnológico (CNPq), da Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), da Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), da Fundação de Amparo à Pesquisa do Rio de Janeiro (FAPERJ) e do Laboratório Nacional de Computação Científica (LNCC). II AGRADECIMENTOS Há algum tempo eu andava perdido, esgotado e bitolado. Você me salvou, Laura. Ao meu orientador, Augusto Schrank, pelos ensinamentos (não apenas científicos), pela imensa oportunidade, por confiar na minha capacidade e instigar minha criatividade. Ao meu co-orientador, Rafael Guedes, pela presteza e cobrança, sempre estando disponível para eventuais duvidas e trabalhos vindouros. A Profª.Marilene Vainstein por me abrir as portas do laboratório, sem ela eu não estaria aqui. Ao Prof. Charley Christian Staats pela ajuda, ensinamentos e por me aceitar como orientado nos anos vindouros. A Profª. Lívia Kmetzsch Rosa e Silva pela ajuda, ensinamentos e pela revisão da redação científica. A Profª. Ana Tereza Ribeiro de Vasconcelos por me abrir as portas do LNCC e pela imensa gentileza. A Profª. Maristela Pereira que, em conjunto com a Profª. Ana Tereza Ribeiro de Vasconcelos, integrou a comissão de acompanhamento. Aos diversos professores do PPGBCM que sempre me auxiliaram. Aos colegas do laboratório 217, Ângela, Eder, Thaís, Alexia e Paola, que resistem fazendo biologia molecular de fungos filamentosos e me instigam. Aos colegas dos laboratórios 220 e 222, que de alguma maneira contribuíram para o desenvolvimento desse trabalho. Aos diversos colegas, professores e amigos que contribuíram, não apenas no mestrado, mas durante a graduação e outras etapas da minha vida. Ao Luciano e a Silvinha, pelo auxílio durante o Mestrado Em especial a minha família, pelo apoio e investimento na minha formação. III SUMÁRIO 1 RESUMO ............................................................................................................................. VII 2 ABSTRACT ....................................................................................................................... VIII 3 REVISÃO BIBLIOGRÁFICA .............................................................................................. 1 3.1 Controle Biológico .................................................................................................................. 1 3.1.1 O carrapato bovino Rhipicephalus microplus e seu Controle Biológico ............................ 2 3.2 O modelo de estudo Metarhizium spp. .................................................................................. 5 3.2.1 Características e Taxonomia de Metarhizium anisopliae e do Gênero Metarhizium ........ 5 3.2.3 Evolução da ordem Hypocreales, família Clavicipitaceae e do gênero Metarhizium ..... 11 3.2.4 Interação Metarhizium-Hospedeiro .................................................................................... 15 3.2.5 Metabólitos secundários de fungos e sua importância no gênero Metarhizium .............. 21 3.2.6 A interação Metarhizium anisopliae-Rhipicephalus microplus explorada por métodos transcritômicos ................................................................................................................. 26 4 JUSTIFICATIVA ................................................................................................................. 30 5 OBJETIVOS ......................................................................................................................... 31 5.1 Objetivo Geral ...................................................................................................................... 31 5.2 Objetivos Específicos ............................................................................................................ 32 6 RESULTADOS ..................................................................................................................... 33 6.1 Manuscrito: Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: Genome identification and patterns of expression in a cuticle infection model ................................................................................................................................. 33 6.2 Arquivos Suplementares do Manuscrito: ........................................................................... 54 7 DISCUSSÃO ....................................................................................................................... 130 8 CONCLUSÕES E PERSPECTIVAS ............................................................................... 136 9 REFERÊNCIAS BIBLIOGRÁFICAS ............................................................................. 138 IV LISTA DE FIGURAS Figura 1: Ciclo de vida do carrapato bovino Rhipicephalus microplus. R. microplus se caracteriza por ser um exo-parasita monóxeno, com um ciclo de vida que compreende um período parasitário e outro de vida livre. O período parasitário dura em média 3 semanas, se iniciando com as larvas que se alimentam até chegar a fase adulta. Pós-cúpula a fêmea aumenta consideravelmente a ingesta de sangue, intumescendo e se desprendendo do animal. Uma vez no solo, a fêmea amadurece seu sistema reprodutivo a fim de ovipositar. ................. 5 Figura 2: Aspecto morfológico da linhagem E6 de Metarhizium anisopliae. (A) Colônia em Meio de Cove Completo (MCc). (B) Do micélio hialino emergem os conidióforos que darão origem aos conídios de coloração verde-musgo (C). Imagem de autoria de Arruda e colaboradores (Arruda et al., 2005). ........................................................................................... 7 Figura 3: Diferenças morfológicas entre linhagens de Metarhizium anisopliae. (A) AL; (B) M5; (C) MT; (D) E6; (E) E9; (F) Rjd; (G) Nordeste; (H) CARO7; (I) CARO11; (J) CARO12; (K) CARO14; (L) CARO19; (M) CG27; (N) CG30; (O) CG31; (P) CG33. Modificado de Schrank & Vainstein (Schrank e Vainstein, 2010). ........................................... 9 Figura 4: Divergência temporal das maiores famílias da ordem Hypocreales. Calibração das divergências foi baseada em um parasita fúngico (supostamente pertencente a ordem Hypocreales) encontrado aderido ao corpo de um inseto fossilizado do período Cretáceo. As cores agrupam os prováveis estilos de vida/ traços nutritivos das linhagens ancestrais e de espécies atuais. Modificado de Sung e colaboradores (Sung et al., 2008). .............................. 11 Figura 5: Ciclo infeccioso de Metarhizium anisopliae. (1, 2, 3) Adesão do conídio à superfície do hospedeiro, germinação e diferenciação em apressório; (4) Penetração; (5) Blastosporos na hemolinfa do artrópode; (6) Colonização do artrópode; (7) Extrusão das hifas do cadáver mumificado do artrópode; (8) Conídios e conidióforos sobre a superfície do cadáver mumificado do artrópode. CO- conídio, GT- tubo germinativo, AP- apressório, H- hifa, PP- penetração. Modificado de Schrank & Vainstein (Schrank e Vainstein, 2010). ....... 16 Figura 6: Vias de infecção, crescimento e reprodução de diferentes fungos entomopatogênicos. (a) Enquanto fungos das ordens Entomophthorales, Neozygitales e Hypocreales iniciam sua infecção através da carapaça, fungos da ordem Onygenales desenvolvem a infecção pós-ingestão de conídios pelo hospedeiro. (b) Crescimento de hifas pós-penetração. (c) Liberação de conídios no ambiente. Modificado deBoomsma e colaboradores (Boomsma et al., 2014). .................................................................................... 17 LISTA DE TABELAS Tabela 1: Exemplos de genes diferencialmente expressos nas comparações pareadas do ensaio transcritômico conduzido por Staats e colaboradores (2014) para M. anisopliae. 28 V LISTA DE ABREVIATURAS h Horas °C Graus Celsius pH Potencial hidrogeniônico MS Metabólito Secundário ITS Internal transcribed spacers EF-1α Elongation factor 1-alpha β-tub Beta-tubulina RPB1 DNA-directed RNA polymerase II subunit RPB1 RPB2 DNA-directed RNA polymerase II core subunit RPB2 SABIA System for Automated Bacterial Integration of Annotation Mya million years ago: milhões de ano atrás HGT horizontal gene transfer: transferência horizontal gênica MP Metabólito primário
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