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College of Agriculture Microbiomes of the Amazon Forest University of Sao Paulo “Luiz de Queiroz” College of Agriculture Microbiomes of the Amazon forest: bacterial diversity and community structure in the phyllosphere, litter and soil Julio Cezar Fornazier Moreira Thesis presented to obtain the degree of Doctor in Science. Area: Soil and Plant Nutrition Piracicaba 2018 Julio Cezar Fornazier Moreira Agricultural and Environmental Engineer Microbiomes of the Amazon forest: bacterial diversity and community structure in the phyllosphere, litter and soil Advisor: Prof. Dr. MARCIO RODRIGUES LAMBAIS Thesis presented to obtain the degree of Doctor in Science. Area: Soil and Plant Nutrition Piracicaba 2018 2 Dados Internacionais de Catalogação na Publicação DIVISÃO DE BIBLIOTECA – DIBD/ESALQ/USP Moreira, Julio Cezar Fornazier Microbiomes of the Amazon forest: bacterial diversity and community structure in the phyllosphere, litter and soil / Julio Cezar Fornazier Moreira. - - Piracicaba, 2018. 95 p. Tese (Doutorado) - - USP / Escola Superior de Agricultura “Luiz de Queiroz”. 1 Interações planta-bactéria 2. Florestas tropicais 3. 16S rRNA 4. Biodiversidade 5. Seca I. Título 3 This thesis is dedicated to my family for their love, endless support and encouragement. 4 ACKNOWLEDGMENTS Special thanks to my parents, Terezinha and Elviro and my brother, Augusto, who supported and advised my journey. My fiancee Ellen, thank you a lot for everything, you were my support to overcome every hard moment, thank you for all your affection and dedication. I love you so much! I would like to acknowledge the College of Agriculture “Luiz de Queiroz”, University of Sao Paulo (ESALQ/USP) for the knowledge and support. Thanks for the Molecular Microbiology Laboratory group under the coordination of Dr. Marcio Rodrigues Lambais. Prof. Dr. Marcio Lambais, I’m grateful for the opportunity to be part of this great group, thanks also for all the advises and time that you spent with me, mostly guiding me to achieve this degree. I would like to thank Prof. Dr. Jorge Luiz Mazza Rodrigues, for helping me at the University of California – Davis, where I have conducted part of my PhD. Thank you for the valuable time that you have spent for the development of my work. Thanks Professors Dra. Luciana F. Alves, Dr. Bruno Henrique Pimentel Rosado and Dr. Rafael Silva Oliveira for all suggestions, valuable discussions and advices. Thank you my friends, Mauro, Lidiane, André and Silvia for all your help, you were essential on this journey, thanks for the partnership in the field sampling and the valuable discussions. I would like to say thanks to Prof. Dra. Rosa Mourão and Lais from UFOPA/Santarém, who spared no effort to help us during field sampling. In Santarem, I’d like to say thanks also to the Flona Tapajós team, specially to Louro Lima for his especial dedication and delicious dishes during the field sampling days. Thanks to my lab friends in Brazil, Adriano, Alice, Elisa, Bianca, Endrews, Felipe, Eric and in Davis Rachel, Jordan, Jonathan, Alonna, Alexandre Rosado, Alexandre Pedrinho and Fernanda. I would like say thanks also to the lab techinicians Wladimir, Nivanda, Denise and Fernado for all support. Thanks to my friends in Piracicaba, Fabio, and Alice, and especially to the little Eva, who always gladdens our meetings. Thanks to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) for the scholarship granted in Brazil at the beginning of my Doctorate. I would like to say thanks to the Sao Paulo Research Foundation (FAPESP) for the scholarships FAPESP Grant number: 2016/15932-4 and 2017/14968-0. 5 CONTENT RESUMO ............................................................................................................................................................... 6 ABSTRACT ........................................................................................................................................................... 7 1. INTRODUCTION ............................................................................................................................................. 9 REFERENCES...................................................................................................................................................... 11 2. HOST AND PLANT FUNCTIONAL TRAITS DRIVE PHYLLOSPHERE AND SOIL BACTERIAL COMMUNITY STRUCTURE IN THE AMAZON RAINFOREST .............................................................. 15 ABSTRACT ......................................................................................................................................................... 15 2.1. INTRODUCTION ........................................................................................................................................... 15 2.2. MATERIAL AND METHODS .......................................................................................................................... 17 2.2.1. Study area .......................................................................................................................................... 17 2.2.2. Leaf and soil sampling ....................................................................................................................... 18 2.2.3. Host plant traits determination ........................................................................................................... 18 2.2.4. Leaf microbial cell dislodgment ........................................................................................................ 19 2.2.5. Soil physicochemical analyses ........................................................................................................... 20 2.2.6. DNA extraction, 16S rRNA gene amplification, and sequencing ...................................................... 20 2.2.7. Sequence analyses .............................................................................................................................. 21 2.2.8. Data analysis and statistics ................................................................................................................. 22 2.3. RESULTS ..................................................................................................................................................... 23 2.3.1. The bacterial communities in the phyllopshere and rhizosphere of Amazonian trees are distinct ..... 23 2.3.2. Host species are drivers of bacterial community structure in the phyllosphere of Amazonian trees . 30 2.3.3. There are indicator bacterial taxa for most of the Amazonian tree phyllospheres ............................. 32 2.3.4. The core microbiome of the phyllosphere of Amazonian trees ......................................................... 34 2.3.1. Phyllosphere and rhizoshere bacteriomes are constrained by plant traits and soil attributes ............. 37 2.3.2. Habitat filtering favor unique functional microbial traits .................................................................. 42 2.4. DISCUSSION ................................................................................................................................................ 44 REFERENCES...................................................................................................................................................... 50 3. EXTREME CLIMATIC EVENTS HAVE DIFFERENTIAL IMPACTS ON THE BACTERIAL COMMUNITIES OF THE PHYLLOSPHERE, LITTER AND RHIZOSPHERIC SOIL IN THE AMAZON RAINFOREST .................................................................................................................................. 57 ABSTRACT ......................................................................................................................................................... 57 3.1. INTRODUCTION ........................................................................................................................................... 57 3.2. MATERIAL AND METHODS .......................................................................................................................... 60 3.2.1. Study area .......................................................................................................................................... 60 3.2.2. Leaf, litter and soil sampling .............................................................................................................. 61 3.2.3. Host plant traits determination ........................................................................................................... 61 3.2.4. Leaf and litter microbial cell dislodgment ......................................................................................... 62 3.2.5. Soil physicochemical analysis ........................................................................................................... 63 3.2.6. DNA extraction, 16S rRNA gene amplification, and sequencing ...................................................... 63 3.2.7. Sequence analyses and statistics ........................................................................................................ 64 3.3. RESULTS ..................................................................................................................................................... 65 3.3.1. Richness and diversity of bacterial communities in the phyllosphere, litter and rhizospheric soil .... 65 3.3.2. Bacterial community structure in the phyllopshere, litter and rhizospheric soil ................................ 70 3.3.3. Plant traits and environmental factors as modulator of the bacterial
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