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Spatiotemporal mapping of bacterial membrane potential responses to extracellular electron transfer.

ABSTRACT: Extracellular electron transfer (EET) allows microorganisms to gain energy by linking intracellular reactions to external surfaces ranging from natural minerals to the electrodes of bioelectrochemical renewable energy technologies. In the past two decades, electrochemical techniques have been used to investigate EET in a wide range of microbes, with emphasis on dissimilatory metal-reducing bacteria, such as Shewanella oneidensis MR-1, as model organisms. However, due to the typically bulk nature of these techniques, they are unable to reveal the subpopulation variation in EET or link the observed electrochemical currents to energy gain by individual cells, thus overlooking the potentially complex spatial patterns of activity in bioelectrochemical systems. Here, to address these limitations, we use the cell membrane potential as a bioenergetic indicator of EET by S. oneidensis MR-1 cells. Using a fluorescent membrane potential indicator during in vivo single-cell-level fluorescence microscopy in a bioelectrochemical reactor, we demonstrate that membrane potential strongly correlates with EET. Increasing electrode potential and associated EET current leads to more negative membrane potential. This EET-induced membrane hyperpolarization is spatially limited to cells in contact with the electrode and within a near-electrode zone (<30 ?m) where the hyperpolarization decays with increasing cell-electrode distance. The high spatial and temporal resolution of the reported technique can be used to study the single-cell-level dynamics of EET not only on electrode surfaces, but also during respiration of other solid-phase electron acceptors.

SUBMITTER: Pirbadian S

PROVIDER: S-EPMC7443868 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Spatiotemporal mapping of bacterial membrane potential responses to extracellular electron transfer.

Pirbadian Sahand S Chavez Marko S MS El-Naggar Mohamed Y MY

Proceedings of the National Academy of Sciences of the United States of America 20200803 33

Extracellular electron transfer (EET) allows microorganisms to gain energy by linking intracellular reactions to external surfaces ranging from natural minerals to the electrodes of bioelectrochemical renewable energy technologies. In the past two decades, electrochemical techniques have been used to investigate EET in a wide range of microbes, with emphasis on dissimilatory metal-reducing bacteria, such as <i>Shewanella oneidensis</i> MR-1, as model organisms. However, due to the typically bulk ...[more]

PMID: 32747561

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Project description:To exchange electrons with extracellular substrates, some microorganisms employ extracellular electron transfer (EET) pathways that physically connect extracellular redox reactions to intracellular metabolic activity. These pathways are made of redox and structural proteins that work cooperatively to transfer electrons between extracellular substrates and the cytoplasmic membrane. Crucial to the bacterial and archaeal EET pathways are the quinol oxidases and/or quinone reductases in the cytoplasmic membrane where they recycle the quinone/quinol pool in the cytoplasmic membrane during EET reaction. Up to date, three different families of quinol oxidases and/or quinone reductases involved in bacterial EET have been discovered. They are the CymA, CbcL/MtrH/MtoC, and ImcH families of quinol oxidases and/or quinone reductases that are all multiheme c-type cytochromes (c-Cyts). To investigate to what extent they are distributed among microorganisms, we search the bacterial as well as archaeal genomes for the homologs of these c-Cyts. Search results reveal that the homologs of these c-Cyts are only found in the Domain Bacteria. Moreover, the CymA homologs are only found in the phylum of Proteobacteria and most of them are in the Shewanella genus. In addition to Shewanella sp., CymA homologs are also found in other Fe(III)-reducing bacteria, such as of Vibrio parahaemolyticus. In contrast to CymA, CbcL/MtrH/MtoC, and ImcH homologs are much more widespread. CbcL/MtrH/MtoC homologs are found in 15 phyla, while ImcH homologs are found in 12 phyla. Furthermore, the heme-binding motifs of CbcL/MtrH/MtoC and ImcH homologs vary greatly, ranging from 3 to 23 and 6 to 10 heme-binding motifs for CbcL/MtrH/MtoC and ImcH homologs, respectively. Moreover, CymA and CbcL/MtrH/MtoC homologs are found in both Fe(III)-reducing and Fe(II)-oxidizing bacteria, suggesting that these families of c-Cyts catalyze both quinol-oxidizing and quinone-reducing reactions. ImcH homologs are only found in the Fe(III)-reducing bacteria, implying that they are only the quinol oxidases. Finally, some bacteria have the homologs of two different families of c-Cyts, which may improve the bacterial capability to exchange electrons with extracellular substrates.

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Spatiotemporal mapping of bacterial membrane potential responses to extracellular electron transfer.

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Spatiotemporal mapping of bacterial membrane potential responses to extracellular electron transfer.

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