Understanding the Physiology of Extracellular Electron Uptake in Purple Nonsulfur Bacteria

Microbially catalyzed oxidation-reduction reactions drive nutrient cycling and energy flux on Earth. Photoautotrophs, which include the cyanobacteria (oxygenic) and purple and green sulfur bacteria (anoxygenic), transform light energy into chemical energy and are responsible for substantial global primary productivity. Anoxygenic phototrophs, in particular, play a crucial role in biogeochemical cycling in anoxic illuminated environments because of their ability to oxidize an array of inorganic compounds for CO2 fixation. Electron donors include molecular hydrogen, nitrite, and reduced sulfur compounds. Recent evidence has also suggested that solid-phase conductive substances (SPCSs), including rust (mixed-valent iron minerals) and their proxies (poised electrodes), can serve as electron donors for anoxygenic phototrophs. This phenomenon is called phototrophic extracellular electron uptake (EEU) and is the reverse process of extracellular electron transfer (EET) performed by metal-reducing bacteria. While numerous examples of microbes performing EET to minerals/electrodes exist and the molecular, physiological, and ecological role of this process is well-studied, very little is understood about EEU. The objectives of this research were to use purple nonsulfur bacteria as a model system to address key knowledge gaps in our understanding of EEU. In Chapter 1, I provide the first experimental evidence that EEU is linked to photosynthetic electron transfer, energy transduction, and the generation of cellular reducing equivalents in the phototrophic Fe(II)-oxidizing bacterium Rhodopseudomonas palustris TIE-1. Furthermore, I show that the Calvin-Benson-Bassham (CBB) cycle (the most broadly distributed CO2 fixation pathway on Earth) is the primary electron sink for phototrophic EEU. In Chapter 2, I expand our understanding of the diversity of organisms known to engage in EEU by isolating and characterizing a new EEU-capable bacterium Rhodovulum sulfidophilum AB26. Using whole-genome- and transcriptome-sequencing, and biochemical approaches, I explore the electron-transfer pathways involved in EEU. This work sets the stage for physiological and genetic studies of this organism. Overall, the findings from this thesis advance our understanding of the physiology of microbial EEU, its diversity, and its role in biogeochemical cycling