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Nitrification: Hunting for Soil Prokaryotes Microbiology

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Nitrification: Hunting for Soil Prokaryotes Microbiology Nitrification: hunting for soil prokaryotes Inês Graça Gonçalves dos Santos Thesis to obtain the Master of Science Degree in Microbiology Supervisors: Professor Rogério Paulo de Andrade Tenreiro Professor Rodrigo da Silva Costa Examination Committee Chairperson: Professor Jorge Humberto Gomes Leitão Supervisor: Professor Rogério Paulo de Andrade Tenreiro Member of the Committee: Professor Ana Cristina Anjinho Madeira Viegas December, 2017 ACKNOWLEDGMENTS This project came out of a collaboration between the Microbiology and Biotechnology Lab (M&B- BioISI) and the Bioclub (cE3c) group. Without the support and dedication of the people involved it would certainly not have been possible. First, I would like to express my deepest gratitude to Professor Rogério Tenreiro, for the incredible opportunity. Thank you for taking me in and supporting me throughout this year, knowing when to push me and when to stand back. My gratitude extends beyond this thesis, for first instilling in me the curiosity which made me choose this path. To Professor Cristina Cruz, I am thankful for the knowledge and for the enthusiastic perspective she never fails to bring, even in the worst days. I would also like to thank the Bioclub group for their contribution to this project. To Professor Rodrigo Costa, for the suggestions and the availability throughout this process. To Professor Ana Tenreiro, for the support, the trust and the patience. Thank you for the unfailing kindness and the helping minions. I would also like to thank the people at M&B-BioISI for all their support. To Professor Lisete for the help and the advice. To Filipa Silva, for maintaining the lab working smoothly. To all the Bugworkers, I owe a tremendous thank you. I was lucky enough to become a part of a group of interested and dedicated people, always willing to help and share. In a line of work in which most days are frustrating and run too long, having people like this makes all the difference. To Ana, Catarina and João, for the company, the sushi in times of despair and the endless puns. To Sofia, for the precious help, the boundless energy and the never-ending questions. To André and Beatriz, for all their help, for the coffee runs and for putting up with my bad temper. To Pedro, for the incredible patience with which he deals with my questions. To Cláudia for taking us under her wing and teaching us all she could. To Jéssica and Miguel, for the cake and the silliness that made it all better. And to Ana Marta and Mariana, the other two vertices of this triangle, for somehow getting me through these years with at least some of my sanity left. Thank you for everything, from the late night impromptu singing to the early morning hugs. I’m so grateful that I got to share it all with you, I couldn’t have done it otherwise. I would also like to thank my friends for their unwavering patience and support, especially during these trying years. To Zé who never stops trying to make me laugh, and to Raquel, for being an inspiration and my safety net my entire life. Lastly, above all, to my family, who created a safe space filled with love and laughter for me to grow and learn, thank you for never allowing me to believe that I couldn’t be or do anything I wanted if I put my mind to it. II ABSTRACT Nitrification, the aerobic oxidation of ammonia to nitrate, is a key part of the N-cycle, bringing about serious ecological and economical concerns. A lot about this process remains unanswered, given the extreme difficulty in isolating ammonia-oxidizers and nitrite-oxidizers. Characterization of ten distinct Portuguese soils through physiochemical and biological features, revealed their different profiles, influencing diversity found. Initial diversity was assessed through an NGS- based microbial profiling analysis. Archaeal-nitrifiers, mainly represented by Nitrososphaera vienensis and “Ca. Nitrosotenuis”, composed almost 100% of detected Archaea; while bacterial-nitrifiers corresponded to a minor proportion of the reads, found only in three samples, represented by Nitrospira, Nitrosococcus and uncultured-AOB. Selective enrichment of diverse nitrifiers from these samples was achieved using different nitrogen + sources for AOB (to cope with NH4 tolerance and urease production), nitrite for nitrite-oxidizers and the + - - addition of antibiotics for archaeal ammonia-oxidizers. Monitoring of NH4 , NO2 and NO3 , complemented with the detection of functional genes, showed that the strategy worked best with lower concentrations of ammonium and in the presence of urea. Communities of AOB, NOB and Thaumarchaeota detected by a multi-probe FISH approach were found clustered together, densely aggregated in a matrix, forming consortia of nitrifiers. Culturable diversity was assessed through M13-PCR fingerprinting of the 477 isolates obtained from the enrichments for bacterial-nitrifiers. Identification of a few representative isolates revealed the presence of chemolithoautotrophs and N-cycle bacteria, though no nitrifiers have been identified so far. From these results, the role of microbial communities contributing to N-cycle and their distribution can be evaluated regarding soil type. Key-words: Nitrification; Soil microbial ecology, FISH, Microbial profiling; Genomic fingerprinting. IV RESUMO A nitrificação é um processo ecológico inserido no ciclo do azoto que corresponde à oxidação consecutiva de amónia a nitrito a nitrato, e ao qual podem ser atribuídas consequências ambientais e económicas severas. Muito é ainda desconhecido sobre este processo, devido à dificuldade em isolar nitrificantes. Dez solos portugueses foram caracterizados físico-química e biologicamente, correlacionando com a diversidade encontrada. Diversidade inicial foi estimada por perfil microbiano baseada em NGS. AOA encontram-se representadas principalmente por Nitrososphaera vienensis e “Ca. Nitrosotenuis”, correspondendo a quase 100% das arqueas detetadas enquanto que para bactérias, nitrificantes correspondem a uma minoria das reads, encontradas apenas em três amostras, representadas por Nitrospira, Nitrosococcus e oxidantes de amónia não-cultivadas. O enriquecimento seletivo de diversos nitrificantes foi feito usando diferentes fontes de azoto para + AOB (para lidar com tolerância a NH4 e produção de urease), nitrito para oxidantes de nitrito e antibiótico + - - para arqueas oxidantes de amónia. Doseamento de NH4 , NO2 e NO3 , juntamente com deteção de genes funcionais, revelou que a estratégia funcionou melhor na presença de ureia ou de menores concentrações + de NH4 . Comunidades de AOB, NOB e Thaumarchaeota detetadas por FISH com multi-sondas, foram encontradas agregadas numa matriz, formando consórcios de nitrificantes. A diversidade cultivável foi estimada por M13-PCR fingerprinting dos 477 isolados obtidos dos enriquecimentos para bactérias nitrificantes. Identificação de alguns isolados representativos permitiu detetar quimiolitotróficos e bactérias associadas ao ciclo do N, mas nenhum nitrificante foi identificado até agora. A partir destes resultados, o papel das comunidades microbianas a contribuir para o ciclo do azoto e a sua distribuição podem ser avaliadas por tipo de solo. Palavras-chave: Nitrificação; Ecologia Microbiana do Solo; FISH; Perfil microbiano; Fingerprinting genómico. V INDEX Acknowledgments ............................................................................................................................................ II Abstract .......................................................................................................................................................... IV Resumo ............................................................................................................................................................ V Figure Index ..................................................................................................................................................... X Tables Index ................................................................................................................................................... XII Abbreviation list ............................................................................................................................................ XIV Nitrification: from the organisms to the process .............................................................................................. 3 1. Nitrogen cycle: an overview ....................................................................................................................... 3 1.1 Nitrogen fixation ................................................................................................................................... 4 1.2 Mineralization and immobilization ....................................................................................................... 4 1.3 Nitrification ........................................................................................................................................... 5 1.4 Anaerobic ammonia oxidation .............................................................................................................. 5 1.5 Heterotrophic nitrification .................................................................................................................... 5 1.6 Denitrification ....................................................................................................................................... 6 2. Diversity and phylogeny of nitrifiers .........................................................................................................
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