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Pinpointing the Origin of Mitochondria

Wang, Zhang
Thesis/Dissertation; Online
Wang, Zhang
Wu, Martin
The explosive growth of genomic data presents both opportunities and challenges for the study of evolutionary biology, ecology and diversity. Genome-scale phylogenetic analysis (known as phylogenomics) has demonstrated its power in resolving the evolutionary tree of life and deciphering various fascinating questions regarding the origin and evolution of earth’s contemporary organisms. One of the most fundamental events in the earth’s history of life regards the origin of mitochondria. Overwhelming evidence supports the endosymbiotic theory that mitochondria originated once from a free-living α-proteobacterium that was engulfed by its host probably 2 billion years ago. However, its exact position in the tree of life remains highly debated. In particular, systematic errors including sparse taxonomic sampling, high evolutionary rate and sequence composition bias have long plagued the mitochondrial phylogenetics. This dissertation employs an integrated phylogenomic approach toward pinpointing the origin of mitochondria. By strategically sequencing 18 phylogenetically novel α-proteobacterial genomes, using a set of “well-behaved” phylogenetic markers with lower evolutionary rates and less composition bias, and applying more realistic phylogenetic models that better account for the systematic errors, the presented phylogenomic study for the first time placed the mitochondria unequivocally within the Rickettsiales order of α-proteobacteria, as a sister clade to the Rickettsiaceae and Anaplasmataceae families, all subtended by the Holosporaceae family. Using this refined mitochondrial phylogeny as framework, gene content reconstruction provides strong evidence that the last common ancestor of mitochondria and α-proteobacteria is an obligate endosymbiont possessing an ATP/ADP translocase that imports ATP from the host, which directly contrasts with the current role of mitochondria as the cell’s energy producer. In addition, it was predicted to possess a flagellum and be capable of oxidative phosphorylation under low oxygen condition. Our ancestral state reconstruction shines light on the driving force of the initial endosymbiosis event. We find features consistent with the “oxygen scavenger hypothesis” but no support for the alternative “hydrogen hypothesis”. Furthermore, characterization of individual bacterial genomes provides valuable insights into bacterial predation and endosymbiosis in general.
University of Virginia, Department of Biology, PHD, 2014
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