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Open Maresca Thesis F.Pdf The Pennsylvania State University The Graduate School Eberly College of Science THE GENETIC BASIS FOR PIGMENT VARIATION AMONG GREEN SULFUR BACTERIA A Thesis in Biochemistry and Molecular Biology by Julia A. Maresca Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2007 The thesis of Julia A. Maresca was reviewed and approved by the following committee members* Donald A. Bryant Ernest C. Pollard Professor of Biotechnology and Professor of Biochemistry and Molecular Biology Thesis Advisor Chair of Committee John H. Golbeck Professor of Biochemistry and Biophysics Sarah E. Ades Assistant Professor of Biochemistry and Molecular Biology Squire J. Booker Associate Professor of Biochemistry and Molecular Biology Lee R. Kump Professor of Geosciences Robert A. Schlegel Professor of Biochemistry and Molecular Biology Department Head, Department of Biochemistry and Molecular Biology *Signatures are on file with the Graduate School ii Abstract The pigmentation differences between green-colored and brown-colored green sulfur bacteria (GSB) are more than cosmetic: species with different pigmentation inhabit different parts of the photic zone. Green-colored species, which make bacteriochlorophyll (BChl) c or d as their primary antenna BChl and chlorobactene as their main carotenoid, tend to be found in the upper layer of anaerobic photic zones. Brown-colored species, which make BChl e and the dicyclic carotenoid isorenieratene, are usually found deeper in the water column. These pigment pairs are invariant, which means that for a green species to become a brown one or vice versa, changes in two unrelated biosynthetic pathways must occur. In this work, comparative genomics has been used to identify the genes unique to pigment biosynthesis in green-colored and brown-colored green sulfur bacterial species. The gene encoding the C-20 methyltransferase, responsible for the difference between BChls c and d, has been identified and inactivated, and detailed analysis of BChl c- and d- producing strains has provided a molecular explanation for the observation that BChl c-containing species tend to live in darker environments. Additionally, a cluster of genes found exclusively in the genomes of brown-colored GSB species has been identified, and fragments of this cluster have been inserted into the chromosome of Chlorobium (Chl.) tepidum to investigate their role in BChl e biosynthesis. Using phylogenetic profiling, carotenoid cyclases specific to chlorobactene or isorenieratene biosynthesis were identified. These cyclases are responsible for the difference between mono- and dicyclic carotenoids, and their activity has been characterized both in GSB and in a heterologous expression system in Escherichia coli. Based on these analyses, the biosynthetic pathway for chlorobactene was established and a similar pathway for isorenieratene biosynthesis is demonstrated. Lastly, analysis of genome regions has identified chlorobactene-modifying enzymes which synthesize the membrane-associated OH-chlorobactene acyl glycosides in both green-colored and brown-colored GSB. These genes have been inactivated in Chl. tepidum and their roles in synthesizing glycosylated and acylated carotenoids have been confirmed. The investigations described in this work explain the genetic basis for stratification of green- colored species in the environment, complete the biosynthetic pathway for chlorobactene, identify the first known isorenieratene-specific carotenoid cyclase, and explain some of iii the natural variation in carotenoid end products seen in different species of green sulfur bacteria. Four of these proteins, the carotenoid cyclases, the carotenoid glycosyltransferase, and the carotenoid acyltransferase, are the first-characterized members of what appear to be large families of carotenoid-modifying enzymes. iv Table of Contents List of Tables x List of Figures xi Acknowledgements xiv CHAPTER 1. Introduction. 1 1.1 Green sulfur bacteria 2 1.2 Phylogeny of green sulfur bacteria 2 1.3 Ecology of green sulfur bacteria 4 1.4 Carbon and sulfur metabolism 5 1.5 Bacteriochlorophylls in the chlorosome: the antenna of green sulfur bacteria 6 1.6 (Bacterio)chlorophylls associated with the chlorosome baseplate, the FMO protein, and the photosynthetic reaction center. 8 1.7 Carotenoids in green sulfur bacteria 9 1.8 Genome sequences of green sulfur bacteria 10 1.9 Identification of genes unique to pigment biosynthesis in green sulfur bacteria 12 CHAPTER 2. Identification of a new class of carotenoid cyclases in photosynthetic organisms 38 Abstract 39 2.1 Introduction 40 2.2 Methods 2.2.1 Bacterial strains and growth conditions 43 2.2.2. Phylogenetic profiling 43 2.2.3 Preparation of genomic library and identification v of gene 43 2.2.4 Construct for inactivation of cruA (CT0456) in Chl. tepidum 44 2.2.5 Pigment analysis 44 2.3 Results 2.3.1 Phylogenetic profiling 45 2.3.2 Identification of lycopene cyclase in Chl. tepidum 45 2.3.3 Inactivation of Lycopene Cyclase in Chl. tepidum 45 2.3.4 Phylogenetic Analyses of Lycopene Cyclases 46 2.4 Discussion 47 2.5 References 50 CHAPTER 3. Heterologous expression of CruA-type carotenoid cyclases and proposed biosynthetic pathway for isorenieratene 71 Abstract 72 3.1 Introduction 73 3.2 Methods 3.2.1 Strains and growth conditions 75 3.2.2 Constructs for expression of CruA and CruB in E. coli 75 3.2.3 Assays of CruA and CruB activity in E. coli 75 3.2.4 Expression of cruB in Chl. tepidum 76 3.2.5 Inhibition of carotenoid cyclization 76 3.2.6 Pigment analysis 76 3.3 Results vi 3.3.1 Activity of cruA and cruB on lycopene in E. coli 78 3.3.2 Activity of cruA and cruB on neurosporene in E. coli 78 3.3.3 Expression of cruB in Chl. tepidum 78 3.3.4 Inhibition of lycopene cyclase activity 79 3.4 Discussion 80 3.5 References 84 CHAPTER 4: Identification of two genes encoding carotenoid- modifying enzymes in Chlorobium tepidum 104 Abstract 105 4.1 Introduction 106 4.2 Materials and Methods 4.2.1 Identification of candidate genes and phylogenetic comparisons 107 4.2.2 Construction of mutant strains 108 4.3 Results 4.3.1 Identification of candidate genes for the terminal steps of carotenogenesis in Chl. tepidum 108 4.3.2 Insertional inactivation of CT1987 and CT0976 109 4.3.3 Characterization of mutant strains 109 4.3.4 Growth rates of mutants 110 4.3.5 Sequence comparisons and phylogenetic analyses 110 4.4 Discussion 110 4.5 References 114 CHAPTER 5: Identification of the bacteriochlorophyll c C-20 methyl- transferase in Chl. tepidum 128 vii Abstract 129 5.1 Introduction 130 5.2 Materials and Methods 5.2.1 Strains and growth conditions 132 5.2.2 Inactivation of CT0028 132 5.2.3 Chlorosome preparation and analysis 132 5.2.4 Growth rate measurements 133 5.2.5 Competition experiments 133 5.3 Results 5.3.1 Identification of genes potentially encoding the BChl c C-20 methyltransferase 135 5.3.2 Sequence analysis of bchU and crtF genes 136 5.3.3 Construction and verification of a CT0028 mutant of Chl. tepidum 137 5.3.4 Pigment analysis of Chl. tepidum CT0028 (bchU) mutant 137 5.3.5 Analysis of molar extinction coefficients of BChl c and d 138 5.3.6 Growth characteristics of BChl c and BChl d strains 139 5.3.7 Competition between BChl c- and d- containing strains 139 5.4 Discussion 141 5.5 References 146 CHAPTER 6: Oxidation of the C71 position of bacteriochlorophyll e 166 Abstract 167 viii 6.1 Introduction 168 6.2 Materials and Methods 6.2.1 Genomic comparisons 170 6.2.2 Dot-blot analysis of distribution of putative BChl e- and isorenieratene-specific genes in a culture collection 170 6.2.3 Expression of genes from Pld. phaeoclathrati- forme in Chl. tepidum 170 6.2.4 Pigment analysis 171 6.3 Results 6.3.1 “In silico” subtractive hybridization 171 6.3.2 Distribution of BE1 and cruB among brown- colored species of GSB 172 6.3.3 Expression of genes from Pld. phaeoclathrati- forme in Chl. tepidum 172 6.4 Discussion 173 6.5 References 176 APPENDICES Appendix A. The biochemical basis for structural asymmetry in carotenoids. 196 Appendix B. Genetic manipulation of carotenoid biosynthesis in the green sulfur bacterium Chlorobium tepidum. 231 Appendix C. Attempts to transform Chlorobium phaeobacteroides strain 1549 with exogenous DNA. 243 Appendix D. Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat 264 Appendix E. Identification of a homoserine lactonase in Sulfolobus solfataricus 276 ix Appendix F. Complete curriculum vitae for Julia Maresca 296 x List of Tables Chapter 2. Table 2.1 Primers used Table 2.2 Protocols for HPLC analysis of pigments Chapter 3. Table 3.1 Primers used in this work Table 3.2 Plasmid combinations in E. coli strain BL21(DE3): pAC-LYC Table 3.3 Plasmid combinations in E. coli strain BL21(DE3): pAC-NEUR Chapter 4. Table 4.1 Primers used in this work Chapter 5. Table 5.1 Absorption maxima in vivo and in methanol of bacteriochlorophylls c, d, and e. Table 5.2 Primers used in this work Table 5.3 Growth rates of bacteriochlorophyll c- and d-producing strains of Chl. tepidum and Chl. vibrioforme Chapter 6. Table 6.1 Primers used in this work Table 6.2 Genes possibly specific to BChl e biosynthesis in the region around cruB in the genomes of 3 brown-colored GSB Table 6.3 Distribution of genes BE1 and cruB among green-colored and brown-colored GSB species in a culture collection xi List of Figures Chapter 1. Figure 1.1 Phylogeny of the major eubacterial taxa based on RecA sequences Figure 1.2 Phylogeny of GSB based on 16S rDNA sequences Figure 1.3 Micrograph of Chl. tepidum cells and extracellularly deposited S0 Figure 1.4 Transmission electron micrograph of Chl.
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