Abstract the Acquisition of a Plastid by Haptophytes, Cryptophytes, And
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Abstract The Acquisition of a Plastid by Haptophytes, Cryptophytes, and Photosynthetic Heterokonts by John M. Schreiber November 2014 Director: Jeff McKinnon, PhD DEPARTMENT OF BIOLOGY Red algae and green plants are known to have obtained their photosynthetic organelles, or plastids, through the endosymbiotic adoption of cyanobacteria. It is still widely debated as to how other eukaryotic alga such as haptophytes, cryptophytes, and photosynthetic heterokonts obtained their plastids, although all are believed to be descended from a red alga. In this thesis, genome-level regressions, analyses of residuals, and Fisher’s exact tests were used to determine how these three eukaryotic algal groups obtained their plastids. A phylogeny also was constructed using 11 plastid genes from various red algae, green plants, haptophytes, cryptophytes, and photosynthetic heterokonts. The results from these collective analyses indicate that multiple endosymbiosis events occurred. Furthermore, they show that a plastid was passed from a red alga, first to cryptophytes, then to photosynthetic heterokonts, and finally to haptophytes in a series of endosymbioses. The Acquisition of a Plastid by Haptophytes, Cryptophytes, and Photosynthetic Heterokonts A Thesis Presented to The Faculty of the Department of Biology East Carolina University In Partial Fulfillment of the Requirement for the Degree Master of Science in Biology by John M. Schreiber November 2014 ©Copyright 2014 John M. Schreiber The Acquisition of a Plastid by Haptophytes, Cryptophytes, and Photosynthetic Heterokonts by John M. Schreiber APPROVED BY: THESIS DIRECTOR:_____________________________________________________ John Stiller, PhD COMMITTEE MEMBER:_________________________________________________ Jinling Huang, PhD COMMITTEE MEMBER:_________________________________________________ Carol Goodwillie, PhD COMMITTEE MEMBER:_________________________________________________ Qin Ding, PhD CHAIR OF THE DEPARTMENT OF BIOLOGY: _________________________________________ Jeff McKinnon, PhD DEAN OF THE GRADUATE SCHOOL: _________________________________________ Paul J. Gemperline, PhD Acknowledgment I would like to thank Jipei Yue and Jinling Huang for compiling the genome database and performing the BLAST searches. I would also like to thank Hui Guo and Qin Ding for sorting all of the BLAST result data. I would like to thank my committee members (Drs. Stiller, Huang, Ding, and Goodwillie) for all of their support and guidance. Finally I would like to thank John Stiller for guiding and supporting me throughout all of the stages of this study. TABLE OF CONTENTS LIST OF TABLES...........................................................................................................vii LIST OF FIGURES..........................................................................................................viii CHAPTER 1: INTRODUCTION.....................................................................................1 Levels of plastid endosymbiosis...........................................................................1 Algae that inherited red algal plastids...................................................................3 CHAPTER 2: USE OF REGRESSION ANALYSES TO UNCOVER EVIDENCE OF PAST ENDOSYMBIOSES Introduction..........................................................................................................7 Methods................................................................................................................7 Results ..................................................................................................................8 Summary..............................................................................................................11 CHAPTER 3: FISHERS’S EXACT TESTS Introduction..........................................................................................................14 Methods................................................................................................................15 Results ..................................................................................................................18 Summary..............................................................................................................20 CHAPTER 4: PLASTID GENE PHYLOGENY Introduction..........................................................................................................23 Methods................................................................................................................23 Results ..................................................................................................................25 Summary..............................................................................................................26 CHAPTER 5: GENERAL DISCUSSION AND CONCLUSIONS.................................27 REFERENCES.................................................................................................................62 APPENDICES..................................................................................................................66 LIST OF TABLES 1. Description of cryptophytes, photosynthetic heterokonts, and haptophytes...............32 2. BLAST results and studentized residuals using Phaeodactylum tricornutum as the query............................................................................................................................33 3. BLAST results and studentized residuals using Phaeodactylum tricornutum as the query............................................................................................................................34 4. BLAST results and studentized residuals using Ectocarpus siliculosis as the query............................................................................................................................35 5. BLAST results and studentized residuals using Aureococcus anophagefferens as the query............................................................................................................................36 6. BLAST results and studentized residuals using Pythium ultimum as the query..........37 7. BLAST results and studentized residuals using Phytophthora infestans as the query............................................................................................................................38 8. BLAST results and studentized residuals using Emiliania huxleyi as the query.........39 9. BLAST results and studentized residuals using Guillardia theta as the query...........40 10. Fisher’s exact tests for signal from red algae in heterokonts......................................41 11. Fisher’s exact tests for signal from cryptophytes in heterokonts................................42 12. Fisher’s exact tests for signals in Emiliania huxleyi...................................................43 13. Fisher’s exact tests for photosynthetic or non-photosynthetic heterokonts in Emiliania huxleyi..........................................................................................................................44 LIST OF FIGURES 1. DNA transfer during endosymbiosis...........................................................................45 2. Proposed models of endosymbiosis by the Chromalveolate hypothesis.....................46 3. Broad phylogenetic analysis........................................................................................47 4. Phylogeny that contradicts the Chromalveolate hypothesis........................................48 5. Linear regression of Phaeodactylum tricornutum BLAST results..............................49 6. Linear regression of Thalassiosira pseudonana BLAST results.................................50 7. Linear regression of Ectocarpus siliculosus BLAST results.......................................51 8. Linear regression of Aureococcus anophagefferens BLAST results...........................52 9. Linear regression of Pythium ultimum BLAST results................................................53 10. Linear regression of Phytophthora infestans BLAST results......................................54 11. Linear regression of Emiliania huxleyi BLAST results...............................................55 12. Linear regression of Guillardia theta BLAST results.................................................56 13. Proposed model of secondary endosymbiosis.............................................................57 14. Proposed model of tertiary endosymbiosis..................................................................58 15. Proposed model of quaternary endosymbiosis............................................................59 16. Proposed model of serial endosymbiosis.....................................................................60 17. Plastid gene phylogeny................................................................................................61 CHAPTER 1: INTRODUCTION Plastid evolution is currently a very active area of inquiry among phylogenomics researchers. While it is fairly well accepted that green plants and red algae obtained their plastids by the endosymbiotic adoption of cyanobacteria (Bhattacharya & Medlin 1995, Delwiche 1999, Moreira et al. 2000, McFadden 2001, Palmer 2003, Bhattacharya et al. 2004, Matsuzaki 2004, Rodriguez-Ezpeleta et al. 2005, Weber et al. 2006, Reyes-Prieto & Bhattacharya 2007, Reyes-Prieto et al. 2007), it remains unclear how a number of groups of eukaryotic algae became photosynthetic. There are several reasons for this. First, green