MOLECULAR EVOLUTION of the PARASITIC GREEN ALGA, HELICOSPORIDIUM SP. by AUDREY PATRICIA DE KONING B.Sc., the University of North

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MOLECULAR EVOLUTION of the PARASITIC GREEN ALGA, HELICOSPORIDIUM SP. by AUDREY PATRICIA DE KONING B.Sc., the University of North MOLECULAR EVOLUTION OF THE PARASITIC GREEN ALGA, HELICOSPORIDIUM SP. by AUDREY PATRICIA DE KONING B.Sc., The University of Northern British Columbia, 1999 M.Sc., The University of British Columbia, 2002 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES (Genetics) THE UNIVERSITY OF BRITISH COLUMBIA AUGUST 2006 Audrey Patricia de Koning, 2006 ii Abstract Helicosporidia are single-celled obligate endoparasites of invertebrates. They have a unique morphology and infection strategy, which make them unlike any other eukaryote. Molecular data were produced to clarify their phylogenetic relationship and to examine the evolution of their cryptic plastid. Phylogenetic analyses of 69 ribosomal proteins identified from an expressed sequence tag (EST) library showed that Helicosporidia are derived green algae and more specifically, are related to the trebouxiophyte algae. An obligate parasitic lifestyle is rare among plant and algal groups, and because Helicosporidium possesses no pigments and no chloroplast-like structure has been identified, photosynthetic ability has presumably been lost in this organism. I sought to examine the role that a relict plastid might play in Helicosporidium. I identified ESTs of 20 putatively plastid-targeted enzymes that are involved in a wide variety of metabolic pathways. As expected, no components of photosynthesis were found, but components of other metabolic pathways including sulfur metabolism and fatty acid, isoprenoid and heme biosynthesis suggest that Helicosporidium retains its plastid for these functions. The complete plastid genome of this species of Helicosporidium was sequenced and revealed only four protein-coding genes not involved in transcription or translation, with two of these confirming the metabolic functions suggested by the nuclear-encoded, plastid-targeted genes identified from the ESTs. In addition, the Helicosporidium plastid genome is one of the smallest known (37.5 kb). Its reduced size results from loss of many genes commonly found in plastids of other plants and algae (including all proteins that function in photosynthesis), elimination of duplicated genes and redundant tRNA isoacceptors, and minimization of intergenic spaces. The Helicosporidium plastid genome is also highly structured, with each half of the circular genome containing nearly all genes on one strand. Both the structure and content of the plastid genome and the deduced function of the organelle show parallels with the relict plastid found in the malaria parasite, Plasmodium falciparum. These unrelated organisms each evolved from photosynthetic ancestors, and the convergence in form and function of their relict plastids suggest that common forces shape plastid evolution, following the switch from autotrophy to parasitism. iii Table of contents Abstract ...................................................................................................................... ii Table of contents.............................................................................................................iii List of Tables .................................................................................................................. vi List of Figures.................................................................................................................vii Acknowledgements .......................................................................................................viii Co-authorship Statement................................................................................................ ix Chapter 1 – Introduction..................................................................................................1 Literature Review.........................................................................................................1 Lifecycle ...................................................................................................................1 Ecology and diversity ...............................................................................................3 Phylogenetics...........................................................................................................4 Research Objectives....................................................................................................5 Origin of Helicosporidium .........................................................................................6 The function of a plastid in Helicosporidium .............................................................6 The Helicosporidium plastid genome .......................................................................7 References ..................................................................................................................9 Chapter 2 - Expressed sequence tag (EST) survey of the highly adapted green algal parasite, Helicosporidium.........................................................13 Introduction ................................................................................................................13 Methods.....................................................................................................................14 Strains, cultivation, and library construction ...........................................................14 Expressed sequence tag sequencing and analysis................................................15 Results and Discussion..............................................................................................16 EST sequencing.....................................................................................................16 Distribution of functional classes of expressed genes............................................17 iv Novel genes in Helicosporidium .............................................................................20 Phylogeny of Helicosporidium genes. ....................................................................22 Concluding remarks ...............................................................................................27 References.................................................................................................................28 Chapter 3 - Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: functional diversity of a cryptic plastid in a parasitic alga............................30 Introduction ................................................................................................................30 Methods.....................................................................................................................32 Identification and characterization of putative plastid-targeted proteins .................32 Phylogenetic analyses............................................................................................32 Presequence characterization................................................................................33 Results.......................................................................................................................34 Discussion .................................................................................................................39 Functional implications of plastid-targeted proteins in Helicosporidium..................39 Fatty acid metabolism ............................................................................................39 Tetrapyrrole biosynthesis .......................................................................................40 Isoprenoid biosynthesis..........................................................................................41 Amino acid biosynthesis.........................................................................................41 Reducing potential..................................................................................................43 Sulfur assimilation ..................................................................................................44 Comparative plastid reduction in obligate parasites ...............................................47 References.................................................................................................................48 Chapter 4 - The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured.................................54 Introduction ................................................................................................................54 Methods.....................................................................................................................56 Cell culture and genomic DNA isolation .................................................................56 Genome sequencing ..............................................................................................56 Annotation and analyses........................................................................................57 v Results and discussion ..............................................................................................57 Genome size and density of coding regions...........................................................57 Genome structure and organization .......................................................................61 Gene content..........................................................................................................64 The Helicosporidium plastid encodes a minimal set of tRNAs................................67
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