Adaptations to Life on an Oxidizing Planet – insights from the evolutionary ecophysiology of iron-respiring bacteria

Abstract

For more than 1 billion years, life on a young Earth evolved in oceans that were essentially devoid of oxygen (O2) and rich in dissolved, un-oxidized iron (Fe2+). However, with the advent of oxygenic photosynthesis and the ensuing rise in O2, the trajectory of life and its co-evolution with Earth was irrevocably changed; oxidized iron (Fe3+) came crashing out of solution in the form of solid iron (oxyhydr)oxide minerals, the contemporary sulfur cycle’s domination became imminent, and in a foreseeably oxidizing ocean, bioavailable iron became a scarce commodity. Vestiges of these evolutionary contexts persist in almost all life today in the form of hemes, iron-sulfur proteins, and iron-scavenging molecules. The organisms whose evolution was undoubtedly the most dramatically impacted were the iron-respiring prokaryotes; that is, bacteria and archaea that “breathe” iron as a means of gaining energy, either oxidizing it as an electron donor (Fe2+) or reducing it as an electron acceptor (Fe3+). In doing so, these metabolisms and the adaptations that support them can also impact the bioavailability of iron, oxygen, and the biogeochemical cycles of other elements with which they intersect. In today’s generally oxidizing world, iron-respiring metabolisms must contend with challenges brought on by the reactivity between Fe2+ and O2, the cell-impermeability of solid iron-bearing minerals, and the influence of the sulfur cycle on iron. In this thesis, I explore the ecophysiology of iron-respiring bacteria through an adaptive lens to better understand if and how these metabolisms persist in an iron-oxidizing world. In Chapter 1, I examine the chemical footprint of an aerobic iron-oxidizing bacteria, discovering a new feature that enables bacteria to mitigate abiotic iron oxidation and mineralization in their environment. In Chapter 2, I assess the capacity for iron-redox cycling in a sulfur-adapted system, finding that biological iron oxidation could not compete with the biologically-driven sulfidic scavenging of iron. Finally, in Chapter 3, I show that an extracellular electron transfer system known for enabling iron reduction is globally distributed and taxonomically widespread amongst the proteobacteria. My findings suggest that this system has undergone extensive, modular changes that have accrued through both vertical inheritance and horizontal gene transfers.