The evolution of oxygenic photosynthesis in the cyanobacterial phylum led to the irreversible oxidation of the Earth’s atmosphere at the Great Oxidation Event (GOE), ~2.5 – 2.0 billion years ago. While the GOE provides a minimum age for the evolution of oxygenic photosynthesis, there is evidence that oxygenic photosynthesis evolved significantly before the GOE. If this is the case, the oxygenation of the Earth’s atmosphere, and by extension cyanobacterial evolution, must have been delayed by some biotic or abiotic factor(s). My dissertation addresses the hypothesis that early cyanobacteria were restricted to terrestrial environments due to salinity intolerance, and their expansion into the marine environment was the trigger for enhanced global oxygenic photosynthesis and the GOE.
My dissertation evaluates this hypothesis across multiple timescales. The first chapter investigates how phylogenetic methods reconstruct microbial traits versus environmental history in deep time. The second chapter focuses on the physiological timescale to empirically investigate the plasticity of salinity tolerance within multiple taxa of modern cyanobacteria. And the third chapter uses experimental evolution to observe the impacts of salinity selection on the salinity response of cyanobacteria.
To test the implications of ancestral state reconstruction (ASR) methods, I produced simulated trait distributions of salinity optima via two models of evolution. These simulated “modern” distributions were used as the data for testing ASR predictions. I established the range of evolutionary rates that allow for salinity to be reconstructed across the cyanobacterial tree, which are slow in comparison with published estimates of rates from fossil and experimental macroevolution data.
I collated data from scientific papers published over the last 70 years reporting cyanobacterial growth responses to changes in salinity. Upon standardizing this historical dataset, I evaluated differences in responses to salinities across the phylum. Over half of the strains isolated from “terrestrial” habitats grew at salinities above the thresholds (0.5 - 5 ppt) typically used to distinguish between terrestrial and marine environments. They are, however, rationalized in terms of a mechanistic model that relates growth rate to maintenance of osmotic homeostasis.
To evaluate how these responses change on evolutionary timescales, I grew sixteen experimental lineages of the model euryhaline cyanobacterium Synechococcus sp. PCC 7002, inoculated from a genetically homogenous ancestor into 4 treatments, ranging from 10% marine salinity to 100% marine salinity, and serially transferred twice a week. I then evaluated these evolved lineages for changes in their general fitness, as well as changes in their plastic response to varying salinities.
My data on both the physiological and evolutionary response of cyanobacteria to changes in salinity suggests that we need to reevaluate how we consider salinity tolerance as a trait in phylogenetic reconstructions. Salinity does not appear to behave as a discrete trait, and salinity tolerance does not appear to be a trait maintained only by strains regularly exposed to higher salinities. These eco-evolutionary results indicate that our perspective of geobiological records of cyanobacterial evolution and the Great Oxidation Event needs to shift from a focus on salinity tolerance of individual organisms toward consideration of the relative environmental niches (marine versus terrestrial) available on the Archean Earth. While phylogenetics can inform our understanding of the evolutionary trajectories of early life, we must address the challenge of considering not just the modern distribution of traits, but also the variance of those traits over ecological and evolutionary timescales.</p
