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Estudo Taxonômico E Molecular De Zygomycetes Em Excrementos De Herbívoros No Recife, Pernambuco, Brasil

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Estudo Taxonômico E Molecular De Zygomycetes Em Excrementos De Herbívoros No Recife, Pernambuco, Brasil ANDRÉ LUIZ CABRAL MONTEIRO DE AZEVEDO SANTIAGO Estudo taxonômico e molecular de Zygomycetes em excrementos de herbívoros no Recife, Pernambuco, Brasil Recife-PE 2008 ANDRÉ LUIZ CABRAL MONTEIRO DE AZEVEDO SANTIAGO Estudo taxonômico e molecular de Zygomycetes em excrementos de herbívoros no Recife, Pernambuco, Brasil TESE APRESENTADA AO CURSO DE PÓS-GRADUAÇÃO EM BIOLOGIA DE FUNGOS DO DEPARTAMENTO DE MICOLOGIA, CENTRO DE CIÊNCIAS BIOLÓGICAS, UNIVERSIDADE FEDERAL DE PERNAMBUCO, COMO PARTE DOS REQUISITOS PARA OBTENÇÃO DO GRAU DE DOUTOR EM BIOLOGIA DE FUNGOS. Orientadora: Profª. Drª. Maria Auxiliadora de Queiroz Cavalcanti Co-orientadora: Profª. Drª. Elaine Malosso Recife-PE 2008 II Santiago, André Luiz Cabral Monteiro de Azevedo. Estudo taxonômico e molecular de Zygomycetes em excrementos de herbívoros no Recife, Pernambuco, Brasil / André Luiz Cabral Monteiro de Azevedo Santiago. – Recife: O Autor, 2008. 111 xxx folhas: il., fig., tab. Tese (Doutorado) – Universidade Federal de Pernambuco. CCB. Departamento de Micologia. Programa de Pós-Graduação em Biologia de Fungos, 2008. Inclui bibliografia e anexos. 1. Coprófilos. 2. Dimargaritales. 3. Variabilidade Genética 4. Mucorales. 5. Zoopagales. I. Título. 582.281.2 CDU (2.ed.) UFPE 579.53 CDD (22.ed.) CCB – 2008-190 III IV A minha esposa Bruna, aos meus pais, Vinícius e Ana e irmãos, Felipe, Fernanda e Beatriz por todo apoio, amor e confiança. V AGRADECIMENTOS À professora Dra. Maria Auxiliadora de Queiroz Cavalcanti pela orientação e atenção desde a iniciação científica. À professora Dra. Elaine Malosso pela co-orientação apoio e atenção. À professora Sandra Trufem por toda a ajuda na identificação dos Zygomycetes desde a iniciação científica. À Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) pelo apoio financeiro o qual possibilitou a realização deste trabalho. À coordenação e aos professores do Programa de Pós-Graduação em Biologia de Fungos pelo apoio e ensinamentos. À minha esposa Bruna e aos meus pais Vinícius e Ana e irmãos Felipe, Fernanda e Beatriz pelo carinho, apoio, confiança e compreensão. À professora Leonor Costa Maia pela revisão de dois dos artigos escritos e pelo total apoio durante o todo o curso. Ao Professor Paulo Santos pela ajuda com as análises estatísticas. Às amigas Marielle, Danielle e Liliani e a professora Dra. Neiva Tinti pela importante ajuda com os experimentos de biologia molecular. Aos amigos Dr. Gladstone Silva e Dr. Bartolomeu dos Santos pela essencial ajuda na purificação do rDNA e nas análises dos seqüenciamentos dos espécimes. Aos amigos de turma pela ajuda e agradável convivência durante o curso de Doutorado. Aos amigos do laboratório de Pós-Graduação em Biologia de Fungos: Micheline, Luciana, Ivone, Josilene, Daniele, Sílvia, Flávia e Eduardo pela agradável convivência durante todo o curso. Aos amigos Elisandro, Bruno, Tatiana, Felipe, Marcela e Jadergudson pela amizade e ajuda. Ao amigo Felipe Reis pela ajuda na revisão da língua inglesa em alguns dos trabalhos produzidos. À direção do Zoológico da Reserva de Dois Irmãos pela permissão concedida para a coleta dos excrementos e ao tratador dos animais, Damião dos Santos, pela ajuda nas coletas. Aos demais amigos do Departamento de Micologia por todo apoio e amizade. Aos funcionários do Departamento de Micologia por toda ajuda. VI Aos que, de alguma maneira, contribuíram para a minha formação intelectual e profissional. VII SUMÁRIO Pág. AGRADECIMENTOS VI RESUMO XIII ABSTRACT XIV 1 - INTRODUÇÃO GERAL 1 1.1 - Zygomycetes ........................................................................................................... 3 1.1.1 - Mucorales Schröter ............................................................................................... 4 1.1.2 - Zoopagales Bessey ex R. K. Benjamin. ................................................................ 6 1.1.3 - Dimargaritales R. K. Benjamin, 1979 ................................................................... 7 1.2 - Fungos coprófilos ..................................................................................................... 7 1.3 - Isolamento de Zygomycetes de excrementos ........................................................... 9 1.4 - Taxonomia Molecular ............................................................................................ 14 1.5 - Marcadores moleculares em seqüências gênicas baseados na Reação em Cadeia da Polimerase (PCR)........................................................................................................15 1.6 - Espaçador Interno Transcrito (ITS) do DNA Ribossomal ..................................... 16 1.7 - Genética Molecular dos Zygomycetes ................................................................... 16 1.8 - Variabilidade genética intra-específica nos Zygomycetes ..................................... 17 2 – REFERÊNCIAS BIBLIOGRÁFICAS ................................................................. 19 CAPÍTULO I - Zygomycetes em excrementos de herbívoros do Parque de Dois Irmãos no Recife, Pernambuco, Brasil....................................................................................31 CAPÍTULO II - Variabilidade genética em Mucorales isolados de excrementos de herbívoros no Parque de Dois Irmãos, Recife, Pernambuco Brasil ........................... 56 CAPÍTULO III - Gilbertella persicaria (Mucorales): um novo relato para o Brasil ... 77 CAPÍTULO IV – Pilobolus (Mucoraceae) em excrementos de herbívoros no Recife, Pernambuco, Brasil.....................................................................................................84 VIII SUMÁRIO (CONTINUAÇÃO) CAPÍTULO V - Mucor guilliermondii : uma espécie rara isolada de excrementos de herbívoro nos neotrópicos ........................................................................................... 98 CAPÍTULO VI - Dimargaris : uma nova ocorrência para o continente sul americano..................................................................................................................105 2 - CONCLUSÕES GERAIS ................................................................................. ....110 ANEXOS IX LISTA DE FIGURAS Pág. CAPÍTULO I Figura 1: Número de táxons de Zygomycetes ocorrentes entre junho/2005 e maio/2006 em excrementos de herbívoros da Reserva Ecológica de Dois Irmãos no Recife, Pernambuco, Brasil. A. Em função da pluviosidade média mensal. B. Em função da temperatura média mensal. 44 CAPÍTULO II Figura 1: Análise filogenética de Mucorales isolados de excremento de herbívoros. A árvore é um fenograma de máxima parcimônia baseado em um alinhamento de 520 bases da região ITS do rDNA. Os números nos ramos indicam a porcentagem de recuperação de 1000 “bootstraps” (> 60%). As seqüências obtidas no “GenBank” são precedidas pelos números de acesso. 75 Figura 2 Análise filogenética de Mucorales isolados de excremento de herbívoros. A árvore é um fenograma de “Neighbor Joining” baseado nas distâncias de Kimura-2-parâmetros obtidas de um alinhamento de 520 bases da região ITS do rDNA. Os números nos ramos indicam a porcentagem de recuperação de 10.000 “bootstraps” (> 60%). As seqüências obtidas no “GenBank” são precedidas pelos números de acesso. 76 CAPÍTULO III Figura 1: Gilbertella persicaria A) Esporangióforo com esporângio imaturo; B): Esporangióforo com esporângio imaturo e columela C) Columela; D) Clamidósporos; E, F) Esporangiósporos. Escala: A=25 µm; B=50 µm; C=50 µm, D=25 µm; E=25 µm; F=10 µm. 80 CAPÍTULO IV Figura 1: Pilobolus crystallinus var. crystallinus A) Vesícula subesporangial e esporângio; B) Vesícula subesporangial e columela; C) Trofocisto; D) Esporangiósporos; P. crystallinus var. kleinii E) Vesícula subesporangial e esporângio; F) Vesícula e columela; G) Trofocisto; H) Esporangiósporos; P. crystallinus var. hyalosporus I) Vesícula subesporangial e esporângio; J) Vesícula subesporangial e columela; K) Trofocisto; L) Esporangiósporos; P. lentiger var. lentiger M) Vesícula subesporangial e esporângio; N) Vesícula subesporangial e columela; O) Trofocisto; P) Esporangiósporos. 90 X LISTA DE FIGURAS (CONTINUAÇÃO) Figura 2: Pilobolus lentiger var. minutus A) Vesícula e esporângio; B) Vesícula e columela; C) Trofocisto; D) Esporangiósporos; P. longipes E) Vesícula e esporângio; F) Vesícula e columela; G) Trofocisto; H) Esporangiósporos; P. roridus var. roridus I) Vesícula e esporângio; J) Vesícula e columela; K) Trofocisto; L) Esporangiósporos; P roridus var. umbonatus M) Vesícula e esporângio; N) Trofocisto; O) Esporangiósporos. 94 CAPÍTULO V Figura 1: Mucor guilliermondii A) Esporangióforo com esporângio; B) Esporângio; C) Esporangióforo com columela; D) Esporangiósporos. Escala: A = 40 µm; B = 20 µm; C = 4 µm; D = 5 µm. 101 CAPÍTULO VI Figura 1: Dimargaris bacillispora A, B) Esporóforos e cabeças férteis em diferentes estágios de desenvolvimento; C) Hifa com septo e cavidade lenticular; D) Merosporangiosporos. Escala: A = 25 µm; B = 25 µm; C = 10 µm; D = 5 µm. 108 XI LISTA DE TABELAS Pág. CAPÍTULO I Tabela 1: Alimentação dos herbívoros da Reserva Ecológica de Dois Irmãos no Recife, Pernambuco, Brasil (Dados fornecidos pela administração da Reserva). 36 Tabela 2: Análise química dos excrementos dos herbívoros da Reserva Ecológica de Dois Irmãos no Recife, Pernambuco, Brasil. 36 Tabela 3: Zygomycetes ocorrentes nos excrementos de herbívoros da Reserva Ecológica de Dois Irmãos no Recife, Pernambuco, Brasil. 39 Tabela 4: Freqüência de ocorrência de Zygomycetes nos excrementos de herbívoros da Reserva Ecológica de Dois Irmãos no Recife, Pernambuco,
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