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      An elusive electron shuttle from a facultative anaerobe

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          Abstract

          Some anaerobic bacteria use insoluble minerals as terminal electron acceptors and discovering the ways in which electrons move through the membrane barrier to the exterior acceptor forms an active field of research with implications for both bacterial physiology and bioenergy. A previous study suggested that Shewanella oneidensis MR-1 utilizes a small, polar, redox active molecule that serves as an electron shuttle between the bacteria and insoluble acceptors, but the shuttle itself has never been identified. Through isolation and synthesis, we identify it as ACNQ (2-amino-3-carboxy-1,4-naphthoquinone), a soluble analog of menaquinone. ACNQ is derived from DHNA (1,4-dihydroxy-2-naphthoic acid) in a non-enzymatic process that frustrated genetic approaches to identify the shuttle. Both ACNQ and DHNA restore reduction of AQDS under anaerobic growth in menaquinone-deficient mutants. Bioelectrochemistry analyses reveal that ACNQ (−0.32 V Ag/AgCl) contributes to the extracellular electron transfer (EET) as an electron shuttle, without altering menaquinone generation or EET related cytochrome c expression.

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          In order to survive, we break down food through a series of chemical reactions that release energy to power our cells. In these metabolic reactions, small electrically charged particles called electrons are removed from the food molecule, and transferred, via a series of reactions, to a terminal electron acceptor.

          For humans and many other organisms, oxygen is the terminal electron acceptor. Bacteria generate energy through a similar series of chemical reactions, but many species of bacteria live in environments where oxygen is absent. Some bacteria solve this problem by transferring the electrons released in their metabolic reactions to acceptor compounds in the external environment. These species must therefore employ a small molecule ‘shuttle’ to carry the electrons to the acceptor.

          Previous work has shown the bacterial strain Shewanella oneidensis MR-1 releases a small molecule into its surrounding environment, which serves as its electron shuttle. Despite identifying a mutant strain of MR-1 that cannot produce this shuttle, researchers have been unable to determine the exact chemical identity of this critical molecule.

          Now, Mevers, Su et al. have identified this elusive electron shuttle. This involved growing MR-1 and isolating the active molecule which restores the mutant bacteria’s ability to shuttle electrons. Further experiments characterizing the structure of this compound using techniques involving analytical and synthetic organic chemistry revealed it be a small molecule known as ACNQ.

          Mevers, Su et al. showed MR-1 produces this elusive electron shuttle by releasing a precursor structure into the environment where it spontaneously converts into ACNQ. As a result, there are no genes present in the genome of MR-1 or other bacterial strains that are required for the production of ACNQ. This genetic absence and low production levels of ACNQ has frustrated previous attempts to identify MR-1’s electron shuttle.

          Bacterial metabolism is studied for its applications in bioenergy (producing renewable energy using living organisms) and bioremediation (detoxification of substances using the reactions of bacterial metabolism). A better understanding of bacterial metabolism is thus essential for the continued development of these useful technologies.

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          Most cited references17

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          Extracellular electron transfer mechanisms between microorganisms and minerals.

          Electrons can be transferred from microorganisms to multivalent metal ions that are associated with minerals and vice versa. As the microbial cell envelope is neither physically permeable to minerals nor electrically conductive, microorganisms have evolved strategies to exchange electrons with extracellular minerals. In this Review, we discuss the molecular mechanisms that underlie the ability of microorganisms to exchange electrons, such as c-type cytochromes and microbial nanowires, with extracellular minerals and with microorganisms of the same or different species. Microorganisms that have extracellular electron transfer capability can be used for biotechnological applications, including bioremediation, biomining and the production of biofuels and nanomaterials.
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            METLIN: A Technology Platform for Identifying Knowns and Unknowns

            METLIN originated as a database to characterize known metabolites and has since expanded into a technology platform for the identification of known and unknown metabolites and other chemical entities. Through this effort it has become a comprehensive resource containing over 1 million molecules including lipids, amino acids, carbohydrates, toxins, small peptides, and natural products, among other classes. METLIN's high-resolution tandem mass spectrometry (MS/MS) database, which plays a key role in the identification process, has data generated from both reference standards and their labeled stable isotope analogues, facilitated by METLIN-guided analysis of isotope-labeled microorganisms. The MS/MS data, coupled with the fragment similarity search function, expand the tool's capabilities into the identification of unknowns. Fragment similarity search is performed independent of the precursor mass, relying solely on the fragment ions to identify similar structures within the database. Stable isotope data also facilitate characterization by coupling the similarity search output with the isotopic m/ z shifts. Examples of both are demonstrated here with the characterization of four previously unknown metabolites. METLIN also now features in silico MS/MS data, which has been made possible through the creation of algorithms trained on METLIN's MS/MS data from both standards and their isotope analogues. With these informatic and experimental data features, METLIN is being designed to address the characterization of known and unknown molecules.
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              Secretion of flavins by Shewanella species and their role in extracellular electron transfer.

              Fe(III)-respiring bacteria such as Shewanella species play an important role in the global cycle of iron, manganese, and trace metals and are useful for many biotechnological applications, including microbial fuel cells and the bioremediation of waters and sediments contaminated with organics, metals, and radionuclides. Several alternative electron transfer pathways have been postulated for the reduction of insoluble extracellular subsurface minerals, such as Fe(III) oxides, by Shewanella species. One such potential mechanism involves the secretion of an electron shuttle. Here we identify for the first time flavin mononucleotide (FMN) and riboflavin as the extracellular electron shuttles produced by a range of Shewanella species. FMN secretion was strongly correlated with growth and exceeded riboflavin secretion, which was not exclusively growth associated but was maximal in the stationary phase of batch cultures. Flavin adenine dinucleotide was the predominant intracellular flavin but was not released by live cells. The flavin yields were similar under both aerobic and anaerobic conditions, with total flavin concentrations of 2.9 and 2.1 micromol per gram of cellular protein, respectively, after 24 h and were similar under dissimilatory Fe(III)-reducing conditions and when fumarate was supplied as the sole electron acceptor. The flavins were shown to act as electron shuttles and to promote anoxic growth coupled to the accelerated reduction of poorly crystalline Fe(III) oxides. The implications of flavin secretion by Shewanella cells living at redox boundaries, where these mineral phases can be significant electron acceptors for growth, are discussed.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                24 June 2019
                2019
                : 8
                : e48054
                Affiliations
                [1 ]deptDepartment of Biological Chemistry and Molecular Pharmacology Harvard Medical School BostonUnited States
                [2 ]deptMolecular Foundry Division Lawrence Berkeley National Laboratory, University of California, Berkeley BerkeleyUnited States
                [3 ]deptState Key Laboratory of Bioelectronics, School of Biological Science and Medical Engineering Southeast University NanjingChina
                [4 ]deptDepartment of Microbiology Harvard Medical School BostonUnited States
                [5 ]deptMolecular Biophysics and Integrated Bioimaging Division Lawrence Berkeley National Laboratory, University of California, Berkeley BerkeleyUnited States
                California Institute of Technology United States
                National Institute of Child Health and Human Development United States
                California Institute of Technology United States
                Author notes
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0001-7986-5610
                https://orcid.org/0000-0001-8784-3120
                https://orcid.org/0000-0003-0213-8356
                Article
                48054
                10.7554/eLife.48054
                6687433
                31232690
                a08c48a4-d312-428a-b630-8a77fa134f3c
                © 2019, Mevers et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 29 April 2019
                : 24 June 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: GM086258
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100008460, National Center for Complementary and Integrative Health;
                Award ID: AT980074
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000015, U.S. Department of Energy;
                Award ID: DE-AC02-05CH11231
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: 5F32GM103010
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004543, China Scholarship Council;
                Award ID: 201606090098
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Short Report
                Biochemistry and Chemical Biology
                Microbiology and Infectious Disease
                Custom metadata
                The identification of ACNQ as an extracellular electron shuttle solves a longstanding problem in bacterial physiology and provides new tool for bioenergy development.

                Life sciences
                shewanella oneidensis,extracellular electron shuttle,redox,acnq,none
                Life sciences
                shewanella oneidensis, extracellular electron shuttle, redox, acnq, none

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