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NON-TARGET ANALYSIS of BIOREMEDIATED SOIL Zhenyu

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NON-TARGET ANALYSIS OF BIOREMEDIATED SOIL Zhenyu Tian A dissertation submitted to the faculty at the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Environmental Sciences and Engineering in the Gillings School of Global Public Health. Chapel Hill 2018 Approved by: Michael D. Aitken Wanda M. Bodnar Avram Gold Kun Lu Jason D. Surratt © 2018 Zhenyu Tian ALL RIGHTS RESERVED ii ABSTRACT Zhenyu Tian: Non-target Analysis of Bioremediated Soil (Under the direction of Michael D. Aitken) Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous pollutants of environmental concern. Bioremediation, relying on stimulation of natural microbial degradation processes, is a well-established technology to clean up PAH-contaminated soils. However, bioremediation does not necessarily lead to a reduction in soil toxicity. PAH-contaminated sites are affected by extremely complex mixtures, like coal tar or creosote, and biotransformation products or co- occurring compounds can also contribute to the overall toxicological effects of contaminated soil before and after bioremediation. Therefore, the objective of this dissertation was to use non- target analysis workflows to identify the genotoxic transformation products, important co- occurring pollutants, and the unrecognized biotransformation pathways that could contribute to explain the toxicological effects observed beyond parent PAHs. To identify the source(s) of increased genotoxicity in bioremediated soil, we pursued a non-target analytical approach combining effect-directed analysis (EDA) and metabolite profiling to compare extracts of PAH-contaminated soil before and after bioremediation. A compound with the composition C15H8O2 and four methylated homologues were shown to accumulate as a result of bioreactor treatment, and the C15H8O2 compound was determined to be genotoxic. Its structure was established as a heretofore unidentified α,β-unsaturated lactone, 2H- naphtho[2,1,8-def ]chromen-2-one (NCO), which was confirmed by synthesis. It also accumulated in aerobically incubated soil from two additional PAH-contaminated sites and was iii formed from pyrene by two pyrene-degrading bacterial cultures known to be geographically widespread, underscoring its potential environmental significance. Azaarenes are nitrogen heterocyclic polyaromatic compounds that co-occur with PAHs but have been poorly studied in environmental systems. High resolution mass spectrometry (HRMS) and mass-defect filtering were applied to four PAH-contaminated samples to analyze the their diversity, abundance, and biodegradation behavior. The diversity, relatively high concentrations, and persistence of high-molecular-weight azaarenes were highlighted, and isomer-selective biodegradation was observed. To help elucidate PAH biodegradation pathways and endpoints in contaminated soil, HRMS and stable isotope-assisted metabolomics (SIAM) workflows were tested and applied to a PAH-contaminated soil. Uniformly 13C-labeled fluoranthene, pyrene, or benzo[a]anthracene were spiked into the soil and incubated in microcosms. With SIAM, known and unknown metabolites such as ring-cleavage products and conjugates were detected, and the transformation pathways leading to their formation proposed. iv ACKNOWLEDGEMENTS To my advisor, Prof. Michael D. Aitken: thank you for all the guidance, support, and patience. You taught me what is to be a good scientist and a man of integrity. To my closest collaborator, Dr. Joaquim Vila: thank you for your help and accompany. I miss the coffee breaks and discussions that nourished our research. To my committee members, Prof. Avram Gold: thank you for teaching me chemistry as well as the healthy life style; Prof. Jason D. Surratt: thank you for those challenging questions and great suggestions for career development; Prof. Wanda Bodnar and Prof. Kun Lu: thank you both for your help on the knowledge and skills of mass spectrometry. To my wife, Han Xiao: thank you for your love and sacrifice. You offered me the support in my most helpless moments. To my parents: thank you for the understanding and support, and I am sorry that I am not a good son in respect to the traditional values. To all the collaborators and lab mates that have helped me in my research: Dr. Jun Nakamura, Dr. Zhenfa Zhang, Leonard Collins, Dr. Vyom Sharma, Dr. Xu Tian, Dr. David Singleton, Dr. Miao Yu, Dr. Alden Adrion, Dr. Eric Staunton, Elizabeth Corteselli, and Elisabeth Rehak. To my friends in the ESE department: Tianqu Cui, Jingbo Wang, Ryan Kingsbury, and Emanuele Sozzi. Thank you all for your help! P.S.: If I missed out anyone in the list of acknowledgements, I sincerely apologize and I could do a proper thank you in person, such as a coffee or chocolate. v TABLE OF CONTENTS LIST OF TABLES ......................................................................................................................... xi LIST OF FIGURES ...................................................................................................................... xii CHAPTER 1 INTRODUCTION ............................................................................................. 1 1.1 Specific aims and rationale ....................................................................................... 2 1.2 Dissertation organization .......................................................................................... 4 CHAPTER 2 BACKGROUND ............................................................................................... 5 2.1 PAHs and related compounds in contaminated sites ................................................ 5 2.2 Toxicity and genotoxicity of polycyclic aromatic compounds ................................. 8 2.2.1 Toxicities of parent PAHs .................................................................................. 8 2.2.2 Toxicities of oxy-PAHs ..................................................................................... 9 2.2.3 Toxicities of azaarenes ..................................................................................... 11 2.3 Biotransformation of PAHs and co-occurring compounds ..................................... 12 2.3.1 Bacterial transformation of PAHs .................................................................... 13 2.3.2 Incomplete metabolism of PAHs ..................................................................... 16 2.3.3 PAH metabolites and increased genotoxicity in contaminated soil ................. 17 2.4. Introduction to non-target analysis ........................................................................ 17 vi 2.4.1 Workflow for non-target analysis .................................................................... 17 2.4.2 Effect-directed analysis .................................................................................... 21 2.4.3 Metabolite profiling ......................................................................................... 22 2.4.4 Stable isotope-assisted metabolomics .............................................................. 23 CHAPTER 3 NON-TARGET ANALYIS REVEALS A BACTERIAL METABOLITE OF PYRENE IMPLICATED IN THE GENOTOXICITY OF CONTAMINATED SOIL AFTER BIOREMEDIATION .................................................................................................................... 26 3.1 Introduction ............................................................................................................. 26 3.2 Materials and methods ............................................................................................ 28 3.2.1 Chemicals ......................................................................................................... 28 3.2.2 Soil and bioreactor treatment ........................................................................... 28 3.2.3 Extraction and Fractionation ............................................................................ 29 3.2.4 Bioassay ........................................................................................................... 29 3.2.5 Instrumental analysis ....................................................................................... 30 3.2.6 Purification of NCO and structure identification ............................................. 30 3.2.7 Other biotransformation experiments .............................................................. 31 3.2.8 Data analysis .................................................................................................... 31 3.3 Results and discussion ............................................................................................ 32 3.3.1 Fractionation of soil extracts and selection of genotoxic fraction ................... 32 3.3.2 Metabolite profiling ......................................................................................... 34 3.3.3 Isolation and structural characterization of C15H8O2 ....................................... 37 3.3.4 Source, putative formation pathway, and potential prevalence. ...................... 41 vii 3.3.5 Environmental relevance ................................................................................. 44 CHAPTER 4 DIVERSITY AND ABUNDANCE OF HIGH-MOLECULAR-WEIGHT AZAARENES IN PAH-CONTAMINATED ENVIRONMENTAL SAMPLES ........................ 46 4.1 Introduction ............................................................................................................. 46 4.2 Materials and methods ...........................................................................................
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