Date Approved

12-2016

Document Type

Dissertation

Degree Name

PhD in Cell & Molecular Biology

Department

Molecular Biology

College

Graduate School of Biomedical Sciences

First Advisor

Eric Moss, PhD

Committee Member 1

Randy Strich, PhD

Committee Member 2

Ronald Ellis, PhD

Committee Member 3

Jongmin Nam, PhD

Subject(s)

Annelida; Phylogeny; Computational Biology; Adenosine Triphosphate; Proton-Translocating ATPases; Conserved Sequence; Gene Transfer, Horizontal; Evolution, Molecular

Disciplines

Cell Biology | Computational Biology | Laboratory and Basic Science Research | Life Sciences | Molecular Biology | Molecular Genetics | Other Ecology and Evolutionary Biology | Other Genetics and Genomics

Abstract

Segmented worms (Annelida) are among the most successful animal inhabitants of extreme environments worldwide. An unusual group of Mesenchytraeus worms endemic to the Pacific Northwest of North America occupy geographically proximal ecozones ranging from low elevation temperate rainforests to high altitude glaciers. Along this altitudinal transect, Mesenchytraeus representatives from disparate habitat types were collected and subjected to deep mitochondrial and nuclear phylogenetic analyses. Evidence presented here employing modern bioinformatic analyses (i.e., maximum likelihood, Bayesian inference, multi-species coalescent) supports a Mesenchytraeus “explosion” in the upper Miocene (5-10 million years ago) that gave rise to ice, snow and terrestrial worms, derived from a common aquatic ancestor. Among these ecologically-disparate but genetically-close worms, those maintaining the highest intracellular ATP levels reside permanently on glacier ice (i.e., M. solifugus). A comparative molecular analysis of 11 core structural subunits of the F1Fo-ATP synthase revealed extraordinary conservation across species, with a few notable exceptions. Most strikingly, the ice worm mitochondrial-encoded ATP6 (a) subunit – the "ATP throttle" known to regulate proton flux, hence ATP synthesis – encoded a highly basic, 15 amino acid carboxy-terminal extension likely to have been acquired by lateral gene transfer from an ancestral prokaryote. This insertion is supported by transcriptome raw read reconstruction and independent PCR amplifications from three geographically-distinct ice worm populations, and represents a rare example of a mitochondrial-based gene transfer event. The position and biochemical properties of the extension domain suggest a role in ATP synthase dimerization and/or proton shuttling, both of which would predictably enhance ATP production.

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