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BACTERIAL ENDOPHYTES OF PLANTS USED FOR SOIL RECLAMATION A Thesis Submitted to the College of Graduate and Postdoctoral Studies In Partial Fulfillment of the Requirements For the Degree of Doctor of Philosophy In the Department of Food and Bioproduct Sciences University of Saskatchewan Saskatoon By Eduardo Kovalski Mitter © Copyright Eduardo Kovalski Mitter, February 2018. All rights reserved. PERMISSION TO USE In presenting this thesis in partial fulfillment of the requirements for a Postgraduate degree from the University of Saskatchewan, I agree that the Libraries of this University may make it freely available for inspection. I further agree that permission for copying of this thesis in any manner, in whole or in part, for scholarly purposes may be granted by the professor or professors who supervised my thesis work or, in their absence, by the Head of the Department or the Dean of the College in which my thesis work was done. It is understood that any copying, publication, or use of this thesis/dissertation or parts thereof for financial gain shall not be allowed without my written permission. It is also understood that due recognition shall be given to me and to the University of Saskatchewan in any scholarly use which may be made of any material in my thesis. Requests for permission to copy or to make other use of material in this thesis in whole or part should be addressed to: Head of the Department of Food and Bioproduct Sciences University of Saskatchewan 51 Campus Drive University of Saskatchewan Saskatoon, Saskatchewan, S7N 5A8 Canada OR Dean College of Graduate and Postdoctoral Studies University of Saskatchewan 116 Thorvaldson Building, 110 Science Place Saskatoon, Saskatchewan, S7N 5C9 Canada i ABSTRACT Microorganisms that colonize the plant rhizosphere and root tissues may provide host plants with nutrients, stimulate growth and increase tolerance to abiotic stress. These plant- microbe associations are also being investigated to assist land reclamation in Alberta’s oil sands. However, these newly reconstructed landscapes may be limited by several factors that include low soil nutrient levels, reduced microbial activity and the presence of residual hydrocarbons. This study was designed to assess the bacterial root microbiome of plants growing in oil sands reclamation covers and investigate the potential use of bacterial endophytes in phytoremediation. Soil microbial community structure in these areas was mainly driven by soil total and organic + carbon, NH4 and organic matter. In addition, an assessment of the bacterial root microbiome associated with sweet clover (Melilotus albus) and barley (Hordeum vulgare) strongly suggests that plants have the ability to select for certain soil bacterial consortia. Sweet clover plants were more selective and mainly associated with Sinorhizobium and Rhizobium, whereas Acholeplasma was unique to barley. Furthermore, genera such as Pseudomonas and Pantoea were able to successfully colonize both plants. However, due to the presence of residual hydrocarbons in these areas, plants may rely on association with hydrocarbon degrading endophytes. Therefore, an assessment of unculturable endophytic communities revealed that sweet clover had higher CYP153 gene copy numbers when compared to barley. In addition, a total of 42 endophytic bacteria isolates tested positive for hydrocarbon degrading genes and were further investigated for their application as inoculants. Based on overall growth promoting effects, sweet clover plants and four different bacterial strains were selected for phytoremediation experiments. Despite plant growth inhibition caused by diesel fuel toxicity, an overall higher plant biomass was observed in inoculated plants. However, only at high diesel concentrations did bacterial inoculants enhanced soil hydrocarbon degradation. In conclusion, bacterial species associated with plants growing in reclamation covers were mainly driven by plant factors and this microbiome harbors endophytes that can be potentially used in phytoremediation. In particular, bacterial endophytes such as Pantoea and Pseudomonas species in association with sweet clover plants were shown to successfully reduce petroleum hydrocarbons in soil. ii ACKNOWLEDGMENTS First and foremost, I would like to thank my best friend and my long-time companion, my fiancé Aline. We have faced many challenges moving to a new country leaving all our family and friends behind, but thanks to your support and encouragement this journey has been much better. I am truly thankful to my supervisors. To Dr. Jim Germida, for providing me with support, advice, great opportunities to present my work, and mentoring me through this long journey. To Dr. Renato de Freitas, for his guidance, encouragement and support in times of frustration and joy doing Science. I also greatly appreciate the time and help given by the other members of my committee, Dr. Bobbi Helgason, Dr. Ken Van Rees and Dr. Gordon Putz; along with my graduate chairs Dr. Robert Tyler, Dr. Darren Korber and Dr. Takuji Tanaka. I could not have done any of this work without the help and friendship of many people at U of S. I am grateful for my friends in the Soil Microbiology lab. A very special thanks to Jorge Cordero, Panchali Katalunda, Bethany Templeton, Zayda Morales, Hannah Konschuh, Natalie Blain, Sarah Kuzmicz, Claire Kohout, Akeem Shorunke, Ashebir Godebo, Anisha Biswaray and Avanthi Wijesinghe. I would also like to thank Kris Novak, Marc St. Arnaud, Dr. Jeff Schoenau, Dr. Fran Walley, Dr. Ryota Kataoka, Landon Sealey and Mark Cooke from the department of Soil Science. Also, I want to express my gratitude to Ann Harley, Donna Selby, and Kim Heidinger for their administrative support. Finally, but very important in my life, I would like to thank my parents for teaching me perseverance in my pursuit of personal and professional goals. This research is funded through a collaborative research and development grant between the Natural Sciences and Engineering Research Council of Canada (NSERC) and the FORWARD project based out of Lakehead University, ON. Partners and supporting organizations of the FORWARD project include Canada’s Oil Sands Innovation Alliance (COSIA), Suncor Energy Inc., Canadian Natural Resources Limited, Total E&P Canada Ltd., Syncrude Canada Ltd., Alberta Newsprint Company, Alberta Pacific Forest Industries, Hinton Pulp, Millar Western Forest Products, Slave Lake Pulp, Tervita Corporation, Environment Canada, Oil Sands Research and Information Network, and Alberta Innovates Technology Futures. iii TABLE OF CONTENTS PERMISSION TO USE ............................................................................................................... i ABSTRACT ............................................................................................................................... ii ACKNOWLEDGMENTS ......................................................................................................... iii TABLE OF CONTENTS ........................................................................................................... iv LIST OF TABLES .................................................................................................................... vii LIST OF FIGURES .................................................................................................................... x LIST OF ABBREVIATIONS .................................................................................................. xiv 1. INTRODUCTION ........................................................................................................... 1 2. LITERATURE REVIEW ................................................................................................ 5 2.1 The Alberta Oil Sands ..................................................................................................... 5 2.2 Tailings Management ...................................................................................................... 7 2.3 Reclamation Strategies .................................................................................................... 8 2.4 Soil microbial community function and structure ............................................................. 9 2.5 Plant-microbe interactions ............................................................................................. 12 2.5.1 The rhizosphere microbiome .............................................................................. 13 2.5.2 The endosphere microbiome .............................................................................. 15 2.6 Phytoremediation .......................................................................................................... 17 2.6.1 Advantages and disadvantages ........................................................................... 18 2.6.2 Use of plants and associated microorganisms for hydrocarbon degradation ........ 19 2.7 Ecology of hydrocarbon degrading bacteria ................................................................... 23 2.7.1 Hydrocarbon degradation ................................................................................... 24 2.7.1.1 Aerobic degradation of aliphatic compounds .................................................. 24 2.7.1.2 Aerobic degradation of aromatic compounds.................................................. 27 2.7.1.3 Hydrocarbon degrading genes ........................................................................ 29 3. MICROBIAL COMMUNITIES ASSOCIATED WITH ANNUAL BARLEY
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