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Andreia Filipa Ferreira Salvador Tems Universidade do Minho Escola de Engenharia Andreia Filipa Ferreira Salvador tems Functional analysis of syntrophic rading microbial ecosys LCFA-degrading microbial ecosystems -deg A CF ysis of syntrophic L unctional anal F a Salvador eir err ilipa F eia F Andr 3 1 UMinho|20 outubro de 2013 Universidade do Minho Escola de Engenharia Andreia Filipa Ferreira Salvador Functional analysis of syntrophic LCFA-degrading microbial ecosystems Tese de Doutoramento em Engenharia Química e Biológica Trabalho realizado sob a orientação da Doutora Diana Zita Machado de Sousa e da Doutora Maria Madalena dos Santos Alves outubro de 2013 Autor Andreia Filipa Ferreira Salvador email [email protected] Título da tese Functional analysis of syntrophic LCFA-degrading microbial ecosystems Orientadores Doutora Diana Zita Machado de Sousa Doutora Maria Madalena dos Santos Alves Ano de conclusão 2013 Doutoramento em Engenharia Química e Biológica É AUTORIZADA A REPRODUÇÃO INTEGRAL DESTA TESE APENAS PARA EFEITOS DE INVESTIGAÇÃO, MEDIANTE AUTORIZAÇÃO ESCRITA DO INTERESSADO, QUE A TAL SE COMPROMETE. Universidade do Minho, 1 de outubro de 2013 ________________________________________ iii AGRADECIMENTOS São muitos aqueles a quem devo um profundo agradecimento por me terem acompanhado e apoiado durante este percurso quer profissionalmente como pessoalmente. Agradeço em primeiro lugar às minhas orientadoras Diana Sousa e Madalena Alves. O optimismo, a força e o rigor com que agarram a investigação são inspiradores. Foi um privilégio ter desenvolvido este projecto convosco. Também merecem um agradecimento especial o Théodore Bouchez e a Ariane Bize do Irstea (França) que se envolveram neste tema e colaboraram sempre com dedicação e entusiasmo. A todos os co-autores deste trabalho um muito obrigado, nomeadamente à Ana Julia Cavaleiro, à Ana Guedes, à Sónia Barbosa, à Juliana Ramos, à Alcina Pereira, ao Alfons Stams, ao Théodore Bouchez, à Ariane Bize, à Madalena Alves e à Diana Sousa pelo trabalho, dedicação e discussões que promoveram. Também gostaria de agradecer a todos aqueles que se foram cruzando comigo no laboratório e nos corredores no Departamento de Engenharia Biológica, em especial aos meus colegas do BRIDGE, e também do Irstea. Um especial agradecimento à Madalena Vieira, à Tânia Ferreira, à Chrystelle Bureau, à Celine Madigou e à Laëtitia Cardona por toda a ajuda técnica. Aos meus colegas de doutoramento com quem partilhei o gabinete e com os quais se geraram conversas muito interessantes num espírito de entreajuda e partilha de conhecimentos. Um agradecimento muito especial às colegas e grandes amigas do “Clube secreto das amigas cientistas”. Sem vocês, não teria sido tão agradável! Ao Bruno por toda a atenção, carinho, companheirismo e interesse no meu trabalho e pelo grande apoio nas alturas mais difíceis. E por último um grande agradecimento à minha família, em especial à minha mãe pelo amor e apoio incondicionais. Sem vocês esta tese não existiria. Muito obrigada! iv The work presented in this thesis was financially supported by a research grant (SFRH/BD/48960/2008) from the Portuguese Foundation for Science and Technology (FCT) and European Social Fund (POPHQREN), and by the project FCOMP-01-0124-FEDER-014784, financed by the FEDER funds through the Operational Competitiveness Programme (COMPETE) and by national funds through the Portuguese Foundation for Science and Technology (FCT). v ABSTRACT Anaerobic degradation of long-chain fatty acids (LCFA), is not yet completely understood. Previous studies suggest that different microorganisms might be involved in the degradation of saturated and unsaturated LCFA and that these compounds inhibit severely the microbial activity, especially the methanogenic activity. In this study, the toxic effect of saturated- (palmitate (C16:0) and stearate (C18:0)) and unsaturated-LCFA (oleate (C18:1)), towards pure cultures of hydrogenotrophic methanogens was evaluated by measuring cells viability and methanogenic activity of Methanospirillum hungatei and Methanobacterium formicicum. The presence of hydrogenotrophic (M. formicicum and M. hungatei) and acetoclastic (Methanosaeta concilii and Methanosarcina. mazei) methanogens in oleate and palmitate enrichment cultures was detected by PCR-DGGE fingerprinting techniques. Acetoclastic methanogens and M. formicicum grew in oleate and palmitate enrichment cultures but M. hungatei only grew in the palmitate’s enrichment. M. hungatei was more sensitive than M. formicicum particularly to unsaturated LCFA. The later was also the most abundant hydrogenotroph detected during the continuous treatment of a synthetic wastewater composed mainly by oleate, as determined by PCR-DGGE. In the same study, M. concilii was identified as the most representative acetoclast. In order to investigate differences between the proteins expressed during the degradation of saturated and unsaturated LCFA, a metaproteomics experiment was designed, in which an anaerobic sludge was incubated with palmitate, stearate and oleate. The same COGs functional categories were identified in the different conditions. The majority of the proteins were assigned to functional categories, energy production and conversion, posttranslational modification and lipid metabolism. Most of the proteins identified belong to Methanosaeta concilli, Syntrophobacter fumaroxidans, Pelobacter propionicus and Pelotomaculum thermopropionicum. Methanosaeta concilii was indeed the most abundant archaea detected by pyrosequencing analysis of the 16S rRNA gene, but the other microorganisms were not even detected by pyrosequencing. Studying metaproteomes of complex microbial communities is still a big challenge especially because most of their genomes are not sequenced which difficult proteins identification. Likewise, when analyzing the proteome of the co-culture, Syntrophomonas zehnderi and M. formicicum, specialized on the degradation of LCFA, M. formicicum’s proteome could be much better characterized compared to S. zehnderi’s, since the genome of a very close related strain of the former is available in public databases and the genome of S. zehnderi is not. S. zehnderi was a dominant microorganism in oleate degrading enrichment cultures under methanogenic and non-methanogenic conditions, stablishing close relationships with hydrogenotrophic methanogens and homoacetogenic bacteria, respectively. vi vii RESUMO Os ácidos gordos de cadeia longa (AGCL) podem ser convertidos a metano por digestão anaeróbia. Contudo, aspectos relacionados com a microbiologia desta conversão ainda não estão completamente compreendidos. Estudos anteriores sugerem que diferentes microrganismos possam estar envolvidos na degradação de AGCL saturados e insaturados e ainda que os AGCL inibem a actividade microbiológica e de forma mais severa a actividade metanogénica. Neste trabalho foi avaliado o efeito toxico dos ACGL saturados (palmitato (C16:0) e estearato (C18:0)) e insaturados (oleato (C18:1)) sobre culturas puras de Methanobacterium formicicum e Methanospirillum hungatei monitorizando a sua viabilidade celular e actividade metanogénica. A presença destes organismos hidrogenotróficos bem como de dois organismos acetoclásticos, Methanosaeta concilii e Methanosarcina mazei, em culturas mistas enriquecidas em degradadores de palmitato e de oleato, foi determinada por PCR-DGGE. Todos permaneceram nos dois enriquecimentos com excepção do M. hungatei que não foi capaz de crescer no enriquecimento com oleato. Este microrganismo mostrou ser mais sensível do que o M. formicicum aos AGCL insaturados, segundo os resultados de viabilidade celular e actividade metanogénica. Em reactores anaeróbios alimentados com um efluente sintético, composto maioritariamente por ácido oleico, M. formicicum e M. concilii foram identificados como os metanogénicos predominantes. Foi efectuado um estudo de metaproteómica com o objectivo de detectar diferenças na expressão de proteínas por parte de uma cultura mista a crescer em AGCL saturados e insaturados. A maioria das proteínas identificadas nos vários ensaios estava relacionada com processos metabólicos de produção de energia, incluindo o metabolismo dos lípidos, e modificação pós-traducional. A maioria das proteínas identificadas corresponde a proteínas dos seguintes microrganismos: Methanosaeta concilli, Syntrophobacter fumaroxidans, Pelobacter propionicus e Pelotomaculum thermopropionicum. Estas amostras foram paralelamente classificadas taxonomicamente com base nos resultados de pirosequenciação do gene que codifica para a subunidade 16S do rRNA. Segundo esta análise a Methanosaeta concilii foi identificada como o organismo metanogénico mais dominante, contudo, não foram detectadas sequências correspondentes a S. fumaroxidans, P. propionicus ou P. thermopropionicum. A falta de informação genética/proteica sobre os microrganismos envolvidos na degradação de AGCL dificulta a identificação de proteínas que poderão ser relevantes neste processo. Analisou-se também a expressão proteica de dois organismos sintróficos, Syntrophomonas zehnderi and M. formicicum, que convertem os AGCL a metano. Neste caso particular foi possível obter uma melhor caracterização do proteoma de M. formicicum do que de S. zehnderi, consequência do facto de apenas o genoma de uma estirpe próxima do primeiro se encontrar sequenciado. A S. zehnderi foi identificada como uma bactéria dominante em culturas especializadas na degradação de oleato quer em condições metanogénicas, estabelecendo relações de sintrofia com microorganismos metanogénicos
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