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Open Thweattetd1.Pdf The Pennsylvania State University The Graduate School CHARACTERIZATION OF PIGMENT BIOSYNTHESIS AND LIGHT-HARVESTING COMPLEXES OF SELECTED ANOXYGENIC PHOTOTROPHIC BACTERIA A Dissertation in Biochemistry, Microbiology, and Molecular Biology and Astrobiology by Jennifer L. Thweatt 2019 Jennifer L. Thweatt Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2019 ii The dissertation of Jennifer L. Thweatt was reviewed and approved* by the following: Donald A. Bryant Ernest C. Pollard Professor in Biotechnology and Professor of Biochemistry and Molecular Biology Dissertation Advisor Chair of Committee Squire J. Booker Howard Hughes Medical Investigator Professor of Chemistry and Professor of Biochemistry and Molecular Biology Eberly Distinguished Chair in Science John H. Golbeck Professor of Biochemistry and Biophysics Professor of Chemistry Jennifer L. Macalady Associate Professor of Geosciences Timothy I. Miyashiro Assistant Professor of Biochemistry and Molecular Biology Wendy Hanna-Rose Professor of Biochemistry and Molecular Biology Department Head, Biochemistry and Molecular Biology *Signatures are on file in the Graduate School iii ABSTRACT This dissertation describes work on pigment biosynthesis and the light-harvesting apparatus of two classes of anoxygenic phototrophic bacteria, namely the green bacteria and a newly isolated purple sulfur bacterium. Green bacteria are introduced in Chapter 1 and include chlorophototrophic members of the phyla Chlorobi, Chloroflexi, and Acidobacteria. The green bacteria are defined by their use of chlorosomes for light harvesting. Chlorosomes contain thousands of unique chlorin molecules, known as bacteriochlorophyll (BChl) c, d, e, or f, which are arranged in supramolecular aggregates. Additionally, all green bacteria can synthesize BChl a, the and green members of the phyla Chlorobi and Acidobacteria can synthesize chlorophyll (Chl) a. The biosynthetic pathways leading to the chlorophylls (Chls) and bacteriochlorophylls (BChls) of green bacteria have been nearly fully elucidated over the past two decades. The current state of knowledge of the biosynthetic pathways leading from protoporphyrinogen IX to the production of the (B)Chls found in green bacteria, and the distribution of these biosynthetic enzymes across the green bacteria in relation to their physiology, is reviewed Chapter 2. The biosynthetic pathway leading to BChlide e or f was known prior to this work, with the exception of one reaction, and the enzyme required for this reaction is characterized in Chapter 3. A gene encoding a putative radical S-adenosyl-L-methionine (SAM) protein, bciD, was known to be required for BChl e biosynthesis in vivo; however, it was unknown whether BciD was sufficient to convert BChlide c into BChlide e. To determine the function of BciD a His-tagged version of the enzyme was produced in Escherichia coli, and the enzyme was characterized. Characterization of BciD iv indicated that it contains a [4Fe-4S] cluster. Biochemical assays showed that BciD catalyzed the conversion of SAM into 5ʹ-deoxyadenosine and BChlide c or d into BChlide e or f, respectively. Additionally, a 71-(OH) BChlide c or d intermediate was also observed. These data led to the conclusion that BciD is a radical SAM enzyme that converts the methyl group of BChlide c or d into the formyl group of BChlide e or f likely via a mechanism involving consecutive hydroxylation reactions of the methyl group. The demonstration that BciD is sufficient to catalyze the conversion of BChlide c into BChlide e completed the biosynthetic pathways for (B)Chl biosynthesis in green bacteria. Additionally, in the process of writing a review of (B)Chl biosynthesis in green bacteria, it became necessary to perform bioinformatic analyses to identify (B)Chl biosynthetic genes in newly available genomes and to validate prior annotations. These data are presented in Chapter 4, where special attention is paid to the enzymes involved in the following reactions: the anoxic coproporphyrinogen III oxidative decarboxylation, protoporphyrinogen (Protogen) IX oxidation, Proto IX magnesium chelation; C13 propionate methylation of Mg-Proto IX, oxidative ring cyclization of Mg-Proto IX 13- monomethyl ester to form the isocyclic E-ring of the macrocyle, C3 vinyl hydration, C8 and C12 methylation, and esterification of (B)Chlides with alcohol pyrophosphates. Finally, Chapter 5 focuses on the photosynthetic pigments and light harvesting complexes of a new Thiohalocapsa sp. that was isolated from Mushroom Spring in Yellowstone National Park. This organism is referred to as Thiohalocapsa MS throughout Chapter 5 and is the first thermophilic member of the genus Thiohalocapsa and only the third thermophilic species purple sulfur bacteria. The main light-harvesting pigments are identified as bacteriochlorophyll a, spirilloxanthin, and anhydro- v rhodovibrin. Additionally, two spectral variants of the peripheral light-harvesting complex, LH2, were identified and co-purified from this organism, they are denoted B800-B830 and B800-B855. The core light harvesting complex, LH1-RC, was also purified and shown to have an absorbance maximum around 900 nm. The near-IR absorbance of this LH1-RC experiences a blue shift of 5-8 nm in response to the loss of Ca2+ ions, similar to other thermophilic purple sulfur bacteria. These results support the hypothesis that, like other thermophilic PSB, the Thiohalocapsa MS LH1-RC complex binds Ca2+ ions that enhance its thermostability. Together the studies presented in this dissertation provide new insights into the light-harvesting pigments and physiology of specific anoxygenic phototrophs and provide a jumping off point for further work on these subjects. vi TABLE OF CONTENTS List of Figures xiii List of Tables xv List of Abbreviations xvi Acknowledgements xix Chapter 1 Introduction to Green Bacteria ........................................................................... 1 1.1 Abstract ............................................................................................................. 2 1.2 Introduction ....................................................................................................... 3 1.3 Light Harvesting in Green Bacteria .................................................................. 8 1.4 Chlorophylls and Bacteriochlorophylls of Green Bacteria ............................. 11 1.5 Organization of This Dissertation ................................................................... 15 References ............................................................................................................. 17 Chapter 2 Biosynthesis of Chlorophylls and Bacteriochlorophylls in Green Bacteria ..... 30 2.1 Abstract ........................................................................................................... 31 2.2 Introduction ..................................................................................................... 32 2.3 Early Steps ...................................................................................................... 32 2.4 Protoporphyrin IX to Chlorophyllide a........................................................... 36 2.4.1 Magnesium Chelation ........................................................................... 36 2.4.2 C13 Propionate Methylation ................................................................. 38 2.4.3 Isocyclic E-Ring Formation .................................................................. 39 vii 2.4.5 Reduction of C17=C18 Double Bond .................................................. 41 2.4.6 Reduction of C8 Vinyl Group .............................................................. 42 2.5 Chlorophyllide a to Bacteriochlorophyllide a ................................................ 45 2.5.1 Reduction of the C7=C8 Double Bond................................................. 46 2.5.2 Hydration of the C3 vinyl group........................................................... 48 2.5.3 3-Hydroxyethyl Dehydrogenase ........................................................... 49 2.6 Chlorophyllide a to Bacteriochlorophyllide c, d, e, and f ............................... 50 2.6.1 Demethoxycarbonylation of the C132 methylcarboxyl group .............. 50 2.6.2 Methylation at C8 and C12 ................................................................... 52 2.6.3 Hydration of the C31 Position ............................................................... 53 2.6.4 Methylation of the C20 methine bridge ................................................ 56 2.6.5 Formation of the C7 Formyl Group of BChlide e ................................ 58 2.7 The final steps in (B)Chl biosynthesis ............................................................ 59 2.7.1 Esterification of (B)Chlide ................................................................... 59 2.7.2 Reduction of the alcohol moiety ........................................................... 63 2.8 Concluding Remarks ....................................................................................... 65 References ............................................................................................................. 66 Chapter 3 Characterization of BciD from Cba. limnaeum ............................................... 82 3.1 Abstract ........................................................................................................... 83 viii 3.2 Introduction ....................................................................................................
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