Abstract
Extracellular electron uptake (EEU) is the ability of microbes to take up electrons from solid-phase conductive substances such as metal oxides. EEU is performed by prevalent phototrophic bacterial genera, but the electron transfer pathways and the physiological electron sinks are poorly understood. Here we show that electrons enter the photosynthetic electron transport chain during EEU in the phototrophic bacterium Rhodopseudomonas palustris TIE-1. Cathodic electron flow is also correlated with a highly reducing intracellular redox environment. We show that reducing equivalents are used for carbon dioxide (CO2) fixation, which is the primary electron sink. Deletion of the genes encoding ruBisCO (the CO2-fixing enzyme of the Calvin-Benson-Bassham cycle) leads to a 90% reduction in EEU. This work shows that phototrophs can directly use solid-phase conductive substances for electron transfer, energy transduction, and CO2 fixation.
Highlights
Extracellular electron uptake (EEU) is the ability of microbes to take up electrons from solidphase conductive substances such as metal oxides
Using TIE-1 as a model system we show that EEU is linked to the photosynthetic electron transport chain, and that this process leads to cells becoming highly reduced with respect to both the intracellular nicotinamide adenine dinucleotide [NAD(H)] and nicotinamide adenine dinucleotide phosphate [NAD(P)(H)] pools
It is unknown if electrons from a cathode enter the photosynthetic electron transport chain (pETC) and if this activity is important for the establishment of a proton motive force (PMF), ATP synthesis, or the generation of reducing equivalents
Summary
Extracellular electron uptake (EEU) is the ability of microbes to take up electrons from solidphase conductive substances such as metal oxides. Anoxygenic phototrophs, which include the green and purple sulfur bacteria, are metabolically versatile microbes that oxidize an array of inorganic compounds[2] These include H2S, H2, Fe2+, and intriguingly, solid-phase conductive substances (SPCSs) via a process called extracellular electron uptake (EEU)[3,4,5]. Our laboratory[3,10], and others[11,12], have recently applied BESs to better understand the molecular details of microbial phototrophic EEU This has led to the discovery of at least two pure cultures capable of EEU from electrodes, the anoxygenic phototrophs Rhodopseudomonas palustris TIE-13 and Prosthecochloris aestuarii[12]. Our results trace the path of electrons following EEU through the electron transport chain and cellular metabolism
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