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METABOLIC EVOLUTION in GALDIERIA SULPHURARIA By METABOLIC EVOLUTION IN GALDIERIA SULPHURARIA By CHAD M. TERNES Bachelor of Science in Botany Oklahoma State University Stillwater, Oklahoma 2009 Submitted to the Faculty of the Graduate College of the Oklahoma State University in partial fulfillment of the requirements for the Degree of DOCTOR OF PHILOSOPHY May, 2015 METABOLIC EVOLUTION IN GALDIERIA SUPHURARIA Dissertation Approved: Dr. Gerald Schoenknecht Dissertation Adviser Dr. David Meinke Dr. Andrew Doust Dr. Patricia Canaan ii Name: CHAD M. TERNES Date of Degree: MAY, 2015 Title of Study: METABOLIC EVOLUTION IN GALDIERIA SULPHURARIA Major Field: PLANT SCIENCE Abstract: The thermoacidophilic, unicellular, red alga Galdieria sulphuraria possesses characteristics, including salt and heavy metal tolerance, unsurpassed by any other alga. Like most plastid bearing eukaryotes, G. sulphuraria can grow photoautotrophically. Additionally, it can also grow solely as a heterotroph, which results in the cessation of photosynthetic pigment biosynthesis. The ability to grow heterotrophically is likely correlated with G. sulphuraria ’s broad capacity for carbon metabolism, which rivals that of fungi. Annotation of the metabolic pathways encoded by the genome of G. sulphuraria revealed several pathways that are uncharacteristic for plants and algae, even red algae. Phylogenetic analyses of the enzymes underlying the metabolic pathways suggest multiple instances of horizontal gene transfer, in addition to endosymbiotic gene transfer and conservation through ancestry. Although some metabolic pathways as a whole appear to be retained through ancestry, genes encoding individual enzymes within a pathway were substituted by genes that were acquired horizontally from other domains of life. Thus, metabolic pathways in G. sulphuraria appear to be composed of a ‘metabolic patchwork’, underscored by a mosaic of genes resulting from multiple evolutionary processes. Substitution of genes encoding pathway enzymes also extends to metabolic pathways in other eukaryotic organisms. Specifically, de novo NAD + biosynthesis in eukaryotes, including those possessing a plastid, has been subjected to numerous gene transfer events, some of which were responsible for the establishment of novel metabolic pathways in plastid-bearing eukaryotes. Another characteristic of G. sulphuraria is observed when cultivating the alga in a liquid medium. Under light limiting conditions, G. sulphuraria excretes porphyrins, which fluoresce when illuminated with near-UV wavelengths of light. Examination of the absorption and emission (fluorescence) spectra of the porphyrin mixture led to the hypothesis of spectral shifting, whereby near-UV light that is unusable for photosynthesis is converted into light readily absorbed by phycocyanin, a photosynthetic pigment synthesized by G. sulphuraria . The calculated relative fluorescence quantum yield, i.e., the efficiency at which absorbed photons are re- emitted as fluoresced light, of the excreted porphyrins was lower than to be expected for counteracting light limiting conditions, possibly indicating a different biological function for porphyrin excretion in G. sulphuraria . iii TABLE OF CONTENTS Chapter Page I. INTRODUCTION ......................................................................................................1 An ‘Ancient’ Pathway for de novo NAD + Biosynthesis ..........................................3 G. sulphuraria Excretes Fluorescent Pigments .......................................................5 II. REVIEW OF LITERATURE....................................................................................8 Evolution Shapes Metabolic Pathways and Processes .............................................8 Endosymbiotic Plastid Evolution Fueled Radiation of Photosynthesis .................10 The Sweet Life of G. sulphuraria ..........................................................................14 What Is Metabolism Without Transporters? ..........................................................16 Adaptation via Horizontally Acquired Transporters ..............................................17 Where There’s Life, There’s NAD + .......................................................................18 Galdieria spp. Algae Excrete Porphyrins ..............................................................19 III. METHODOLOGY ................................................................................................22 Metabolic Pathway and Enzyme Annotation .........................................................22 Phylogenetic Tree Construction and Phylogeny Testing .......................................25 G. sulphuraria Liquid Cultures..............................................................................27 Spectroscopy and Relative Fluorescence Quantum Yield .....................................28 IV. FINDINGS .............................................................................................................33 Core Metabolic Pathways in G. sulphuraria .........................................................33 Transport Sugars in G. sulphuraria .......................................................................43 G. sulphuraria Synthesizes Glycogen ...................................................................45 Glycerol: A Link Between Carbohydrates and Lipids ...........................................48 Distinguishing Metabolic Pathways in G. sulphuraria ..........................................51 Methylmalonyl-CoA Pathway .........................................................................52 Terpenoid Biosynthesis ....................................................................................58 Lineage-specific Distribution of de novo NAD + Biosynthesis Pathways ..............61 Evolutionary History of Aspartate Pathway Enzymes ...........................................64 iv Chapter Page Evolutionary History of the Converged Pathway Enzymes ..................................71 Evolutionary History of Kynurenine Pathway Enzymes .......................................78 The Highly Conserved Pathway for Tetrapyrrole Biosynthesis ............................90 Spectral Shifting by Fluorescent Pigments from G. sulphuraria ..........................94 The Basics: Absorption, Emission, and Excitation ................................................95 Absorption and Emission: The Finer Details .........................................................97 Determining Relative Fluorescence Quantum Yield ...........................................100 V. CONCLUSION ....................................................................................................108 The Metabolic Diversity of G. sulphuraria .........................................................108 The Uncertain Extent of Carbon Metabolism in G. sulphuraria .........................110 Life without a Glyoxylate Cycle ..........................................................................111 Gene Transfers Underscore the Evolution of de novo NAD + Biosynthesis ........113 The Aspartate Pathway: Evolutionary Origins in Eukaryotes .............................114 Evolution of the Kynurenine Pathway in Eukaryotes ..........................................117 Impact of Gene Transfers on Metabolic Evolution in Eukaryotes ......................118 Biological Significance of Porphyrin Excretion in G. sulphuraria .....................120 REFERENCES ..........................................................................................................126 APPENDICES ...........................................................................................................137 v LIST OF TABLES Table Page Statistical Analyses of L-aspartate Oxidase Constraint Trees ..................................67 Statistical Analyses of Quinolinate Synthase Constraint Trees ................................70 Statistical Analyses of NNP Constraint Trees ..........................................................73 Statistical Analyses of NMNAT Constraint Trees....................................................75 Statistical Analyses of NAD + Synthase Constraint Trees .........................................77 Statistical Analyses of Tryptophan 2,3-Dioxygenase Constraint Trees ...................80 Statistical Analyses of Indoleamine 2,3-Dioxygenase Constraint Trees ..................83 Statistical Analyses of Kynurenine-3-Monooxygenase Constraint Trees ................86 Statistical Analyses of Kynureninase Constraint Trees ............................................90 Statistical Analyses of HAO Constraint Trees........................................................107 Genome Annotation and Characterized Enzymes Comparison in G. sulphuraria .137 vi LIST OF FIGURES Figure Page Phototrophic & Heterotrophic G. sulphuraria Cells ..................................................1 Metabolic Pathways for de novo NAD + Biosynthesis ................................................4 Fluorescence of Liquid Culture Medium ....................................................................6 Horizontal Gene Transfer Candidate Protein Families ...............................................9 Proposed Phylogeny of Plastid Evolution.................................................................12 Comparison of Total Transporter Proteins Encoded by Eukaryotic Genomes .........17 Cross Point Determination for Optimum Excitation Wavelength ............................29 Linear Regression of Integrated Fluorescence as a Function of Absorbance ...........29 Glycolysis & Gluconeogenesis Pathway
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