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87-Fernanda-Cid.Pdf UNIVERSIDAD DE LA FRONTERA Facultad de Ingeniería y Ciencias Doctorado en Ciencias de Recursos Naturales Characterization of bacterial communities from Deschampsia antarctica phyllosphere and genome sequencing of culturable bacteria with ice recrystallization inhibition activity DOCTORAL THESIS IN FULFILLMENT OF THE REQUERIMENTS FOR THE DEGREE DOCTOR OF SCIENCES IN NATURAL RESOURCES FERNANDA DEL PILAR CID ALDA TEMUCO-CHILE 2018 “Characterization of bacterial communities from Deschampsia antarctica phyllosphere and genome sequencing of culturable bacteria with ice recrystallization inhibition activity” Esta tesis fue realizada bajo la supervisión del Director de tesis, Dr. Milko A. Jorquera Tapia, profesor asociado del Departamento de Ciencias Químicas y Recursos Naturales, Facultad de Ingeniería y Ciencias, Universidad de La Frontera y co-dirigida por el Dr. León A. Bravo Ramírez, profesor titular del Departamento de Ciencias Agronómicas y Recursos Naturales, Facultad de Ciencias Agropecuarias y Forestales, Universidad de La Frontera. Esta tesis ha sido además aprobada por la comisión examinadora. Fernanda del Pilar Cid Alda …………………………………………… ……………………………………. Dr. MILKO JORQUERA T. Dr. Francisco Matus DIRECTOR DEL PROGRAMA DE …………………………………………. DOCTORADO EN CIENCIAS DE Dr. LEON BRAVO R. RECURSOS NATURALES …………………………………………. Dra. MARYSOL ALVEAR Z. ............................................................ Dr. Juan Carlos Parra ………………………………………… DIRECTOR DE POSTGRADO Dra. PAULINA BULL S. UNIVERSIDAD DE LA FRONTERA ………………………………………… Dr. LUIS COLLADO G. ………………………………………… Dra. ANA MUTIS T Dedico esta tesis a mis padres, Lillie Alda Leiva y Fernando Cid Verdugo quienes dedicaron sus vidas a la tarea de enseñar en la Universidad de La Frontera, Temuco-Chile. Abril, 2018 Agradecimientos /Acknowledgements Agradecimientos /Acknowledgements This study was supported by the following research projects: Doctoral Scholarship from Conicyt (no. 21140534) and La Frontera University. Antarctic Chilean Institute Scholarship (code DT_01-13) for Doctoral studies and for the permits given by them to collect plants in Antarctic protected areas n° 125, 126 and 150. International Cooperation project Conicyt-USA code USA2013-0010 and MECESUP FRO1204 also financed this study. I would like also to acknowledge the Doctoral Program in Natural Resources Management and for its academic and economic supports. Especially Dra. Maria de la Luz Mora that encouraged me for doing this graduate studies. I want also to give special thanks to the administrative staff, Mariela Gonzalez and Gladys Oyarzun for their commitment and dedication at any time. I would also like to give special thanks to Dr. Milko Jorquera Tapia for his constant support, patience, dedication and friendship in the development of this thesis in his laboratory. I want to thank also Dr. Fumito Maruyama for his friendship and voluntary support in my thesis and also for all his assistance in my scholarship in Kyoto University-Japan. I want to refer also to Dr. Ralf Greiner for receiving me in Max Rubner Institute in Karlsruhe-Germany, and I want also to give special thanks to Dr. Steffen Graether for his support in my internship in Guelph University in Canada and all his support while writing all papers done in my thesis. In addition, I want also to thank all researchers who have participated as co-authors in our papers, for their collaboration and helpful comments during manuscript revisions. I want to highlight the good vibes received always from laboratory mates; Nitza Inostroza that helped me in the experiments done in my thesis and encouraged me to keep working despite hard situations in life. Ignacio Rilling who helped me in the I Agradecimientos /Acknowledgements phylogenetic analyses of antifreeze protein sequences. Giovanni Larama who helped me in the bioinformatics searches and analysis of antifreeze proteins. Oscar Navarrete who helped me also with antifreeze protein sequences databases. Lorena Lagos and Patricio Barra who supported me always with their previous experience in laboratory and Luis Marileo for his expertise help in DGGE development. Paola Durán for teaching me at the beginning in the laboratory and also, Jacqueline Acuña who was always able to read or give her opinion to improve the work done in laboratory. I will always be grateful to all of you. Finally, thanks to my family for their unconditional love and support. I love you, we are the best team ;). II Abbreviations Abbreviations ACC deaminase = 1-aminocyclopropane-1-carboxylate deaminase AFP = antifreeze protein C = carbon ColAFP = Colwellia sp. SLW05 AFP DGGE = denaturing gradient gel electrophoresis ERIC = enterobacterial repetitive intergenic consensus HCN = hydrogen cyanide IBP = ice binding protein IAA = indole acetic acid INP = ice nucleating/nucleation protein IRI = ice recrystallization inhibition InaA = gene for ice nucleation in Erwinia ananas (= Pantoea ananatis). InaX = gene for ice nucleation in Xanthomonas campestris -like = protein denoted as putative since their activity have not been confirmed experimentally. MpAFP = Marinomonas primoryensis antifreeze protein N = nitrogen NCBI = National Center for Biotechnology Information III Abbreviations P = phosphorus PCR = polymerase chain reaction PGP = plant growth-promoting PV = phenotypically verified TH = thermal hysteresis IV Glossary Glossary ACC deaminase : Is an enzyme from bacteria that converts ACC synthase, a plant precursor of ethylene, to ammonia and α-ketobutyrate compounds that are readily assimilated. Thus the reduction of ethylene levels ameliorates the effect of “stress by ethylene” in plants. Antifreeze protein : A protein that bind to ice crystals by adsorption causing a thermal hysteresis or ice recrystallization inhibition. Ethylene : Hormone from plants that is produced as a response of stress, inducing processes such as senescence, chlorosis, and abscission that may lead to a significant inhibition of plant growth and survival. Hydrogen cyanide : Is a secondary metabolite produced by prokaryotes especially within the phylum Proteobacteria. HCN is a broad-spectrum antimicrobial compound that has been found to be implicated in the suppression of different plant root diseases. Ice binding protein : A protein found in organisms that live at subzero and near-zero temperatures, that binds to ice. Ice-binding proteins include AFPs and proteins that inhibit IRI of ice, and might include proteins that favors ice formation such as INP. Ice nucleating protein : A protein that induces ice formation at high subzero temperatures. Ice recrystallization inhibition : As a consequence of the adhesion of an AFP to ice, ice recrystallization inhibition prevent the generation of large ice crystals by boundary migration of smaller ice crystals. V Glossary Identity percentage : The extent to which two (nucleotide or amino acid) sequences have the same residues at the same positions in an alignment, often expressed as a percentage. Indole acetic acid : It is an auxin, a plant phytohormone involved in plant growth regulation, specifically affects cells division, extension and differentiation. IAA synthesized by bacteria may be involved in plant growth promotion since it has been proven to increase root surface area and length, and thereby provides the plant a greater access to soil nutrients. Median coverage : Average number of reads that include a given nucleotide in the aligned sequences. PGP mechanisms : Have been described in bacteria among other microorganisms to facilitate nutrient uptake by plant, provide defense against pathogens and insects and/or contribute to ameliorate stress in plants, favoring plant development. Psychrophilic bacteria : Microorganisms adapted to live in extremely cold or freezing temperatures Similarity percentage : The extent to which nucleotide or protein sequences are related. Thermal hysteresis : A non-colligative effect as a consequence of the adhesion of an AFP to ice, lowering the freezing point below the melting point of a solution. VI Thesis summary Thesis summary: Frost events generate considerable damages in agriculture world-wide, thus the study of mechanisms present in Antarctic plant-associated microorganisms such as antifreeze proteins (AFP), could represent a source to search and develop natural strategies to ameliorate frost injury and economical losses in agriculture. The phyllosphere microorganisms of Antarctic vascular plants and their potential application in agriculture have not been investigated in detail so far. Thus, the objective of this thesis is to characterize the bacterial communities from Deschampsia antarctica phyllosphere and to identify putative genes encoding for AFP by determining the whole genomes of culturable bacteria showing antifreeze activity. After a general introduction, this thesis contains the information of three consecutive published manuscripts that includes; firstly a review, which was focused on properties from bacterial ice binding proteins (IBP) that regulates ice growth, both AFP and ice nucleating proteins (INPs), and their biotechnological applications, perspectives in agriculture and shows some information regarding this protein sequences deposited in public databases. Secondly, another paper describes the bacterial community structure on the phyllosphere of Deschampsia antarctica plant and evaluate the presence of ice recrystallization inhibition (IRI) activity in these isolates. Through denaturing gradient gel electrophoresis (DGGE) analysis, it was possible to observe differences
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