Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications
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ENVIRONMENTAL MICROBIOLOGY - MINI REVIEW
Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications Dinesh Gupta1 · Michael S. Guzman2 · Arpita Bose1 Received: 30 June 2020 / Accepted: 7 September 2020 © Society for Industrial Microbiology and Biotechnology 2020
Abstract Microbes exchange electrons with their extracellular environment via direct or indirect means. This exchange is bidirectional and supports essential microbial oxidation–reduction processes, such as respiration and photosynthesis. The microbial capacity to use electrons from insoluble electron donors, such as redox-active minerals, poised electrodes, or even other microbial cells is called extracellular electron uptake (EEU). Autotrophs with this capability can thrive in nutrient and soluble electron donor-deficient environments. As primary producers, autotrophic microbes capable of EEU greatly impact microbial ecology and play important roles in matter and energy flow in the biosphere. In this review, we discuss EEU-driven autotrophic metabolisms, their mechanism and physiology, and highlight their ecological, evolutionary, and biotechnological implications. Keywords Extracellular electron uptake (EEU) · Chemoautotrophy · Photoautotrophy · Photoferrotrophy · Biogeochemical cycle
Introduction The microbial envelope is an electrically nonconductive, physically impermeable barrier to insoluble materials (e.g., minerals and electrodes) that partitions the interior metabolic activities of cells from the outer environment [2, 131]. Microbial cells have evolved elaborate mechanisms to extract electrons from insoluble electron donors using a process called extracellular electron uptake (EEU). To accomplish this, microbes use both direct and indirect electron transfer pathways, which typically involve electron transfer proteins, such as multiheme c-type cytochromes. These proteins enable microbes to oxidize solid electron donors and to drive essential metabolic processes [52, 131]. This process permits microbial survival in environments where soluble Dinesh Gupta and Michael S. Guzman contributed equally to this work. * Arpita Bose [email protected] 1
Department of Biology, Washington University in St. Louis, One Brookings Drive, St. Louis, MO 63130, USA
Biosciences and Biotechnology Division, Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, USA
2
electron donors are limiting. Microbial electron exchange with redox-active minerals, or other microbial cells also supports vital ecological processes. Collectively, these processes shape microbial community interactions and influence the geochemistry of the Earth’s surface. Microbes can also use poised electrodes mimicking redox active minerals to drive microbial metabolisms with electricity. A summary of the known diversity of EEU-driven autotrophy in nature is depicted in Fig. 1. EEU mechanisms move electrons from the extracellular space to intracellular electron transport chains. This is generally a
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