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Phd Thesis Benjamin Ricken „Identification of biological sulfonamide degradation“ Von der Fakultät für Mathematik, Informatik und Naturwissenschaften der RWTH Aachen University zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften genehmigte Dissertation vorgelegt von Master of Science in Biotechnologie Benjamin Ricken aus Kleve, Deutschland Berichter: Universitätsprofessor Dr. rer. nat. Andreas Schäffer Prof. Dr. habil. Philippe François-Xavier Corvini Tag der mündlichen Prüfung: 09.03.2018 Diese Dissertation ist auf den Internetseiten der Universitätsbibliothek verfügbar. Table of Contents | 1 Table of Contents Table of Contents ............................................................................................................................................. 1 Abstract ............................................................................................................................................................... 3 Zusammenfassung .......................................................................................................................................... 4 Abbreviations .................................................................................................................................................... 5 1. Introduction .............................................................................................................................................. 7 1.1. Biological degradation of sulfonamide antibiotics ........................................................... 7 1.2. Ipso-substitution: A general mechanism for biological xenobiotic degradation ... 9 1.3. Biological SMX mineralization: Possible downstream pathways ............................ 17 1.4. Antibiotic subsistence ............................................................................................................... 19 1.5. Aim of this thesis ......................................................................................................................... 21 2. Materials & Methods ........................................................................................................................... 22 2.1. Media and Buffer ......................................................................................................................... 22 2.2. Microbiology ................................................................................................................................. 24 2.3. Molecular biology........................................................................................................................ 32 2.4. Analytic ........................................................................................................................................... 35 2.5. Biochemistry ................................................................................................................................. 41 2.6. Bioinformatic methods ............................................................................................................. 48 2.7. Photodegradation Experiment .............................................................................................. 50 3. Results ...................................................................................................................................................... 51 3.1. Phylogenetic analysis of sulfonamide degrading bacterial strains ......................... 51 3.2. Pathway elucidation of biotic sulfonamide degradation ............................................. 52 3.3. SMX enzyme identification ...................................................................................................... 62 3.4. Bioinformatic analysis of SMX enzymes and their protein and gene sequences 70 3.5. Heterologous expression of sad genes in E. coli AE ....................................................... 77 3.6. Degradation studies with E. coli AE SMX-MO ................................................................... 79 3.7. Degradation studies with E. coli AE expressing sadA ................................................... 85 2 | Table of Contents 3.8. Conversion of indole by E. coli AE 4AP-MO ...................................................................... 87 3.9. Kinetic parameters of the FMNR ........................................................................................... 89 3.10. Clarke electrode measurements ........................................................................................... 91 3.11. Resistance of Microbacterium sp. strain BR1 against sulfonamides ....................... 92 3.12. Growth of Microbacterium sp. strain BR1 in artificial urine ...................................... 95 3.13. Photolysis of SMX under simulated sunlight irradiation ............................................. 96 4. Discussion ............................................................................................................................................... 98 4.1. Ipso-attack initiates biological sulfonamide degradation ........................................... 98 4.2. Downstream pathway ............................................................................................................... 99 4.3. Identification of enzymes responsible for SMX degradation ...................................103 4.4. Sulfonamides molecule structure influences biodegradability ..............................105 4.5. Induction of SMX degrading enzymes ...............................................................................108 4.6. Characterization of the FMNR ..............................................................................................109 4.7. Is Microbacterium sp. strain BR1 a potential risk for human health? ..................109 5. Conclusion & Outlook .......................................................................................................................114 6. Publications & Conference proceedings ...................................................................................116 6.1. Publications .................................................................................................................................116 6.2. Oral presentations ....................................................................................................................117 6.3. Poster presentations ................................................................................................................119 7. References ............................................................................................................................................120 8. Appendix ...............................................................................................................................................138 8.1. Declaration of chapters taken from or modified from preprinted publications…………………………………………………………………………………………………138 8.2. Declaration of experimental work conducted and ideas contributed from other persons .............................................................................................................................................139 8.3. Supplementary information .................................................................................................140 Acknowledgements ...................................................................................................................................145 Curriculum vitae ............................................................................... Error! Bookmark not defined. Abstract | 3 Abstract Sulfonamides are among the most administered antibiotics (1), leading to a release of more than 20’000 tons per year into the biosphere (2). Due to their physicochemical properties, they are classified as photolytically- and thermally stable (3). As they do not tend to accumulate or strongly sorb onto organic carbon or other environmental matrices, they move rather freely in the environment (2, 4). Once released, they may enhance the development and the propagation of sulfonamide antibiotic resistance genes (5). Several research groups were able to isolate bacteria being capable of mineralizing different sulfonamide antibiotics (6–10). But, as of yet, the degradation pathway and enzymes involved remained unknown. This work describes the biological degradation of sulfonamide antibiotics by Microbacterium sp. strain BR1. Here, a two-component flavin monooxygenase initiates the degradation by an ipso-attack on the sulfonamide antibiotic. This leads to an electron rearrangement within the molecule and its final decomposition, releasing benzoquinone imine, sulphur dioxide and the heterocyclic moiety as a stable metabolite. Benzoquinone imine is most likely abiotically reduced to 4-aminophenol before it is hydroxylated further by a second two-component flavin monooxygenase, yielding 1,2,4-trihydroxybenzene. Both monooxygenases have so far remained unknown but in this work their genes have also been identified in three other sulfonamide mineralizing bacterial isolates. Growth experiments of Microbacterium sp. strain BR1 cells both acclimatized and non- acclimatized in the presence of the sulfonamide antibiotic sulfamethoxazole indicated that the mineralization of sulfamethoxazole constitutes a new sulfonamide antibiotic resistance mechanism. This is the first report of enzymes involved in the metabolism of antibiotics and the first time that the molecular mechanism of antibiotic subsisting bacteria could be experimentally verified. 4 | Zusammenfassung
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