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Characterization of Diverse Mechanisms of Salicin Degradation in Populus Microbiome Isolates

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Characterization of Diverse Mechanisms of Salicin Degradation in Populus Microbiome Isolates University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 12-2019 Characterization of Diverse Mechanisms of Salicin Degradation in Populus Microbiome Isolates Sanjeev Dahal University of Tennessee, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Recommended Citation Dahal, Sanjeev, "Characterization of Diverse Mechanisms of Salicin Degradation in Populus Microbiome Isolates. " PhD diss., University of Tennessee, 2019. https://trace.tennessee.edu/utk_graddiss/5720 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Sanjeev Dahal entitled "Characterization of Diverse Mechanisms of Salicin Degradation in Populus Microbiome Isolates." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Life Sciences. Jennifer Morrell-Falvey, Major Professor We have read this dissertation and recommend its acceptance: Dale Pelletier, Sarah Lebeis, Cong Trinh, Daniel Jacobson Accepted for the Council: Dixie L. Thompson Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) Characterization of Diverse Mechanisms of Salicin Degradation in Populus Microbiome Isolates A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Sanjeev Dahal December 2019 Dedication I would like to dedicate this dissertation, first and foremost to my family. My father, Mr. Ram Sharan Dahal and my mother, Mrs. Bhagawati Simkhada Dahal always dreamed of providing me with the best education, and they worked hard to bring me opportunities and resources to pursue my dream of becoming a scientist. My brother, Sushant Dahal has always been there as a friend to support me throughout these years. This work is a result of constant encouragement from all the family members and in-laws, and I feel grateful for having them in my life. I also would like to give my deepest gratitude to all the friends here in Knoxville as well as from my alma mater, University of New Orleans. They have given me a second home here in the States and provided me courage and company all the time. Without them, this journey would be very difficult. From University of New Orleans, I would also like to include Dr. Mary J. Clancy who was my first mentor and introduced me to the wonderful world of molecular biology and genetics. Finally, I dedicate my dissertation and express special thanks to my dear wife Susmita Sharma Bajgain for supporting me and encouraging me to successfully complete my PhD. You are my best friend and my inspiration. ii Acknowledgement Numerous people spring to mind, but the first person I would like to thank is my advisor Dr. Dale A. Pelletier. I will forever be indebted to him for teaching me the value of patience and endurance in this field. His guidance on the numerous topics in the thesis was always welcoming. Even when I was at some of the lowest points of my life, he was always there to provide me with kind words and encourage me to move on. I could always go and knock on his door, and he would listen and provide me with positive criticism and ways to make my work better. I believe I have grown not only as a researcher but also as a person because of him. There are several people in the lab to whom I would like to express my gratitude. Tse-Yuan Lu and Leah Burdick have helped me perform several experiments and constantly guided me through laboratory requirements. Previous and current post-doctoral researchers – Collin Timm, Patricia Blair and Dana Carper have also helped me with experiments/analysis and to adjust in the lab. Finally, Aditya Barde, who is a recent Master’s student from the lab, has been a good friend and helped me during enduring times. Some of my collaborators also need to be mentioned here. Dr. Gregory B. Hurst, Dr. Robert L. Hettich and Dr. Suresh Poudel all have been helpful in proteome data generation and analysis. Dr. Timothy J. Tschaplinski, Nancy L. Engle and David Reeves were instrumental in metabolomic assays. Finally, I am thankful to David Garcia who has guided me in several experiments including cell-free reactions and extract preparations. Without the help from the collaborators, I would not be able to make my work as polished as it is. I would also like to express my appreciation to all the committee members – Dr. Sarah L. Lebeis, Dr. Jennifer L. Morrell-Falvey, Dr. Cong T. Trinh and Dr. Daniel A. Jacobson who have been helpful in making sure that my work is as focused as possible. They have been kind and iii critical when required and encouraged me to think like a scientist. Without their guidance, this work would not have been possible. I would also like to thank Dr. Albrecht von Arnim who has provided invaluable advices throughout the years. Finally, I would like to thank everyone in the Genome Science and Technology program especially Teresa Yeatts who has been helpful throughout my stay here. I am also thankful to all the friends and colleagues in the department as well as outside the department who have made my graduate years livelier by bringing me laughs and cheers whenever they could. I am forever grateful. iv Abstract Investigations of metabolic interactions between plant and microbes are vital to designing approaches to promote plant growth and health. Populus, a potential biofuel crop, interacts with its microbiome through numerous metabolites, but research on phenolic glycosides (PGs) is still lacking despite the fact that Populus allocates significant amount of carbon to PGs. Therefore, this study asked the following questions: what is the prevalence of microbiome isolates that utiliZe PGs as growth substrates? what is the diversity in the mechanisms of PG utiliZation? For this study, salicin was used as the model PG substrate. Four naturally occurring salicin degradation systems designated – Bgl, Sal, Lac and Cbg that have been described in literature were investigated in 407 Populus bacterial isolates with available genome sequences. These four systems appear to be present in phylogenetically diverse microbial associates suggesting independent evolution of these mechanisms. Following this, four bacterial strains – Caulobacter sp. AP07, Citrobacter sp. YR018, Agrobacterium rhizogenes OK036 and Rahnella sp. OV744 were selected for further study. Caulobacter sp. AP07 was demonstrated to possess two different salicin systems – Lac and Sal that were both found to be active during growth on salicin minimal media. Citrobacter sp. YR018, on the other hand, utiliZed salicin most likely by gaining mutations. A few possible loci that could have been mutated are proposed in this study. Agrobacterium rhizogenes OK036 was investigated for its unique ability to degrade both the glucosyl and salicyl moieties of salicin unlike other organisms in this study that only utiliZe glucosyl group. Using proteomic, metabolomic and other experimental assays, Agrobacterium was demonstrated to utiliZe salicin by first cleaving glucose off of salicyl alcohol, which is then channeled into gentisate pathway. A few unique features of this novel pathway were explored further using bioinformatic approaches. v Finally, salicin co-metabolism by co-culture of Rahnella sp. OV744 and Pseudomonas sp. GM16 was elucidated. Using proteomic and metabolomic along with other quantitative assays OV744 and GM16 were demonstrated to be involved in a unidirectional cross-feeding interaction during growth on salicin minimal media. The co-culture study illustrates a possible mechanism Populus might utiliZe to fine-tune its microbial coloniZation process. vi Table of contents Chapter 1: Introduction ................................................................................................................. 1 Plant-microbe interactions ..................................................................................................................... 2 Benefits of plant-microbe interactions and their studies .................................................................... 3 Populus as a model for plant-microbe interaction ............................................................................... 5 Phenolic glycosides (PGs) ....................................................................................................................... 6 Importance of PGs .................................................................................................................................. 8 Biosynthesis of PGs ................................................................................................................................. 9 Degradation mechanisms of PGs in Populus-associated microorganisms and their possible role in shaping the Populus microbiome ......................................................................................................... 10 Chapter 2: Phylogenetic and functional diversity in salicin degrading Populus bacterial isolates .........................................................................................................................................
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