Year of Award

2022

Document Type

Thesis

Degree Type

Master of Science (MS)

Degree Name

Cellular, Molecular and Microbial Biology

Other Degree Name/Area of Focus

Microbial Ecology and Evolution

Department or School/College

Division of Biological Sciences

Committee Chair

Scott R. Miller

Commitee Members

Brandon S. Cooper, Jared T. Broddrick

Keywords

thermal adaptation, cyanobacteria, microbial thermophiles, Yellowstone National Park, phylogenomics, metabolic modelling

Subject Categories

Bioinformatics | Computational Biology | Environmental Microbiology and Microbial Ecology | Evolution | Genomics | Microbial Physiology | Molecular Biology | Other Ecology and Evolutionary Biology

Abstract

Thermophilic microorganisms have been scientifically observed since the early nineteenth century and have spurred many questions about the limits of life and the capacity of organisms to survive extreme conditions. Decades of research on thermophile proteins and genomes have yielded several proposed correlates of temperature that may contribute to adaptation of bacteria and archaea to high temperature. However, many of the generalizations reported are drawn from analyses of deeply divergent taxa or from individual case studies in isolation from mesophilic relatives. Members of the Synechococcus A/B (SynAB) group are the only cyanobacteria with members able to grow above 65 °C and represent the most thermotolerant phototrophs on the planet. This group exhibits extensive variation in thermal performance and appears to represent a single adaptive radiation to colonize higher temperature environments—providing an ideal opportunity to test the relative importance of proposed mechanisms of the evolution of thermophily. I have established an unparalleled collection of SynAB strains and genomes from populations in Yellowstone NP and Oregon. Phylogenomics confirmed that lineages of Synechococcus that have diverged in thermotolerance have a unique, ancient origin, and physiological characterization corroborates a pattern of sequential adaptation to increasingly higher temperatures. During adaptation to higher temperatures, SynAB genomes have shrunk dramatically, and I argue that this is likely due to decreases in community complexity rather than selection for smaller cell size or faster growth. Proteome adaptation at the SynAB thermal limit has included the evolution of amino acid composition (most notably, the onset of aspartate phobia) and the acquisition of new proteins from distantly related bacteria. My work also establishes a framework to tackle longstanding questions about the relative contributions of thermodynamic constraints versus biochemical adaptation during the evolution of thermal physiology. To help spur the field of thermal biology in a new direction, I present a novel integration of genomic, physiological, and metabolic modelling approaches that enables exploration of how a cellular system, not just its constituent components, responds to the factors that contribute to the thermal limit of phototrophy.

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© Copyright 2022 Christopher L. Pierpont