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On the Red Algal Genus Grateloupia in the Gulf of Mexico

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On the Red Algal Genus Grateloupia in the Gulf of Mexico ON THE RED ALGAL GENUS GRATELOUPIA IN THE GULF OF MEXICO, FEATURING THE ORGANELLAR GENOMES OF GRATELOUPIA TAIWANENSIS by MICHAEL SCOTT DEPRIEST, JR. JUAN M. LÓPEZ-BAUTISTA, COMMITTEE CHAIR DEBASHISH BHATTACHARYA PHILLIP M. HARRIS MARTHA J. POWELL AMELIA K. WARD A DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biological Sciences in the Graduate School of The University of Alabama TUSCALOOSA, ALABAMA 2015 Copyright Michael Scott DePriest, Jr., 2015 ALL RIGHTS RESERVED ABSTRACT Red algae (Rhodophyta) are economically useful for their gelling compounds, ecologically critical to marine benthic systems, and evolutionarily poised at the intersection of primary and secondary endosymbiotic lineages. Molecular sequencing has transformed our understanding of red algae, revealing genetic and genomic characteristics that had once been completely unknown. In Grateloupia, a red algal genus that is morphologically simple and notoriously difficult-to-identify, sequencing has greatly assisted in identification of species and phylogenetic placement of troublesome taxonomic groups. However, analysis of DNA has also proven useful for genomic comparisons on a larger scale, in order to resolve deep evolutionary questions in terms of overall genome architecture and gene content. Grateloupia is a prime candidate for genomic research, representing an order that had previously not been explored. In this study, sequencing-based analyses were applied at both levels, examining species of Grateloupia both within the genus and from a greater phylogenetic perspective. Phylogenetic analysis of the rbcL marker revealed the previously unknown species Grateloupia taiwanensis, first reporting this non-native alga from the Gulf of Mexico, and it showed that the species previously known as Grateloupia filicina in the Gulf of Mexico actually includes several species. The organellar genomes of Grateloupia taiwanensis were also sequenced and annotated; both the plastid and mitochondrial genome are typical of florideophyte red algae in size, gene content, and structure. Mauve genome alignments demonstrated a pattern of genomic rearrangements expected given the overall phylogeny of Rhodophyta. ii LIST OF ABBREVIATIONS aa Amino acid(s) BI Bayesian inference (of phylogeny) bp Base pair(s) cox1 Cytochrome c oxidase subunit alpha gene DCJ Double-cut-and-join (in Mauve alignments) e or e-value Expect value, used as a statistical significance threshold in BLAST results GC Guanine-cytosine content kb, kbp Kilobase-pairs (1,000 bp) LCB Locally collinear block (in Mauve alignments) ML Maximum likelihood (phylogenetic analysis) ORF Open reading frame rbcL Rubisco-1,5-bisphosphate carboxylase gene s.l. Sensu lato; in the broad sense (in taxonomy) s.s. Sensu stricto; in the strict sense (in taxonomy) iii ACKNOWLEDGMENTS First and foremost, I would like to thank the chairperson of this dissertation, Juan López- Bautista, for inspiring me with the fascinating world of algae since 2008, for his always useful advice on algal and academic issues, and for his patience with me during the preparation of this and other manuscripts. I thank my Ph.D. committee members—Debashish Bhattacharya, Phillip Harris, Martha Powell, and Amy Ward—all of whom have provided unique perspectives and recommendations for my graduate career, and from whom I have learned very much. I also thank my labmates Gabriela Garcia-Soto, Daryl Lam, Trey Melton, Ana Tronholm, and David Ward, who have graciously assisted me with collection trips, new samples of Grateloupia, and/or phylogenetic and genomic analyses. I thank all of my past undergraduate assistants in the PhycoLab, who spent many hours helping me with DNA extractions and reactions. Finally, I sincerely thank Mike Wynne, for his friendly and very detailed advice on the taxonomy of various groups of algae over the years. iv CONTENTS ABSTRACT .................................................................................................................................... ii LIST OF ABBREVIATIONS ........................................................................................................ iii ACKNOWLEDGMENTS ............................................................................................................. iv LIST OF TABLES ......................................................................................................................... vi LIST OF FIGURES ...................................................................................................................... vii 1. Sequencing of the rbcL Marker Reveals the Nonnative Red Alga Grateloupia taiwanensis (Halymeniaceae, Rhodophyta) in Alabama .....................................................................................1 2. Grateloupia filicina Revisited: Molecular Phylogenetics of Grateloupia (Halymeniaceae, Rhodophyta) from the Gulf of Mexico ..........................................................................................14 3. The Plastid Genome of the Red Macroalga Grateloupia taiwanensis (Halymeniaceae) ..........27 4. The Mitochondrial Genome of Grateloupia taiwanensis (Halymeniaceae, Rhodophyta) and Comparative Mitochondrial Genomics of Red Algae ...................................................................46 APPENDIX ....................................................................................................................................70 v LIST OF TABLES 1.1. List of Species Included in Phylogenetic Analysis of Grateloupia taiwanensis ....................13 2.1. List of Species Included in Phylogenetic Analysis of Grateloupia filicina ............................25 2.2. rbcL Pairwise Distances for Selected Grateloupia Species ...................................................26 3.1. Characteristics of Selected Red Algal Plastid Genomes .........................................................42 3.2. List of genes in G. taiwanensis Plastid Genome.....................................................................43 3.3. Comparison of tRNA Sequences in Red Algal Plastid Genomes ...........................................44 3.4. Novel ORFs in the G. taiwanensis Plastid Genome ...............................................................45 4.1 Characteristics of Selected Red Algal Mitochondrial Genomes ..............................................68 4.2. Comparison of Protein-coding Genes in Red Algal Mitochondrial Genomes .......................69 vi LIST OF FIGURES 1.1. Phylogenetic Tree of G. taiwanensis and Related Taxa .........................................................11 1.2. Photograph of G. taiwanensis .................................................................................................12 2.1. Phylogenetic Tree of G. filicina and Related Taxa .................................................................24 3.1. Phylogenetic Tree of Division Rhodophyta ............................................................................39 3.2. G. taiwanensis Plastid Genome ..............................................................................................40 3.3. Pairwise Mauve Genome Alignments of Red Algal Plastid Genomes ...................................41 4.1. G. taiwanensis Mitochondrial Genome ..................................................................................62 4.2. Mauve Genome Alignment of G. taiwanensis and G. angusta ..............................................63 4.3. Mauve Genome Alignment of G. taiwanensis with Rhodymeniophycidae ...........................64 4.4. Mauve Genome Alignment of G. taiwanensis and Sporolithon durum ..................................65 4.5. Mauve Genome Alignment of G. taiwanensis and Pyropia haitanensis ................................66 4.6. Mauve Genome Alignment of G. taiwanensis and Cyanidioschyzon merolae ......................67 vii Sequencing of the rbcL Marker Reveals the Nonnative Red Alga Grateloupia taiwanensis (Halymeniaceae, Rhodophyta) in Alabama ABSTRACT Mobile Bay, AL has been the site for the introduction of several terrestrial and freshwater invasive species, including red imported fire ants (Solenopsis invicta) and spike-topped apple snails (Pomacea bridgesii). The Gulf of Mexico has also been invaded by several marine animal species, such as zebra mussels (Dreissena polymorpha). To date, no invasive marine macroalga has been reported in the Mobile Bay area. However, recent collections of an unusual species of Grateloupia (Halymeniaceae, Rhodophyta) in Alabama indicate that an introduction has been made. On the basis of phylogenetic analysis of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL) marker, the species has been identified as Grateloupia taiwanensis S.M. Lin & H.Y. Liang. This is the first report of G. taiwanensis outside its native range. INTRODUCTION Grateloupia C. Agardh is a genus of benthic marine red algae (Rhodophyta), currently containing about 90 species (Guiry and Guiry, 2012). It is the largest genus in the family Halymeniaceae. Species of this genus occur throughout the world in warm temperate to tropical marine waters. Several Grateloupia species are known in the Gulf of Mexico, specifically Grateloupia gibbesii Harvey and Grateloupia pterocladina (M.J. Wynne) S. Kawaguchi & H.W. Wang, as well as many reports of unidentified Grateloupia species (see Fredericq et al., 2009). Wynne (2011) listed a total of 11 species in the western Atlantic, including G. gibbesii, G. 1 pterocladina, and Grateloupia
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