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      Influence of Incubation Temperature on 9,10-Anthraquinone-2-Sulfonate (AQS)-Mediated Extracellular Electron Transfer

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          Abstract

          The electron shuttling process has been recognized as an important microbial respiration process. Because the incubation temperature can influence both the reactivity of electron mediators and cell growth, it may also affect the electron-shuttle-mediated extracellular electron transfer (EET) process. Here, the effect of incubation temperature (22–38°C) was investigated in a bioelectrochemical system (BES) using Shewanella oneidensis MR-1 and 50 μM of 9,10-anthraquinone-2-sulfonate (AQS). We found that current generation increased as the temperature was increased from 22 to 34°C and then decreased sharply at 38°C. The biofilm biomass, as indicated by the total protein extracted from the electrode, increased as the temperature increased from 22 to 34°C and then decreased at 38°C, mirroring the current generation results. These results were further confirmed by increasing the temperature slowly, step-by-step, in a single BES with a constant biofilm biomass, suggesting that the EET rates could be substantially influenced by temperature, even with the same biofilm. The effects of temperature on the AQS bioreduction rate, c-type cytochrome ( c-Cyts)-bound-cofactor-mediated EET, the AQS mid-point potential, and the AQS diffusion coefficient were studied. From these results, we were able to conclude that temperature influenced the EET rates by changing the c-Cyts-bound-cofactor-mediated EET process and the AQS bioreduction rate, and that the change in biofilm formation was a dominant factor influencing the overall EET rates. These findings should contribute to the fundamental understanding of EET processes. Moreover, optimization of the operating parameters for current generation will be helpful for the practical application of bioelectrochemical techniques.

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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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            Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism

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              Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes

              Dissimilatory reduction of metal (e.g. Fe, Mn) (hydr)oxides represents a challenge for microorganisms, as their cell envelopes are impermeable to metal (hydr)oxides that are poorly soluble in water. To overcome this physical barrier, the Gram-negative bacteria Shewanella oneidensis MR-1 and Geobacter sulfurreducens have developed electron transfer (ET) strategies that require multihaem c-type cytochromes (c-Cyts). In S. oneidensis MR-1, multihaem c-Cyts CymA and MtrA are believed to transfer electrons from the inner membrane quinone/quinol pool through the periplasm to the outer membrane. The type II secretion system of S. oneidensis MR-1 has been implicated in the reduction of metal (hydr)oxides, most likely by translocating decahaem c-Cyts MtrC and OmcA across outer membrane to the surface of bacterial cells where they form a protein complex. The extracellular MtrC and OmcA can directly reduce solid metal (hydr)oxides. Likewise, outer membrane multihaem c-Cyts OmcE and OmcS of G. sulfurreducens are suggested to transfer electrons from outer membrane to type IV pili that are hypothesized to relay the electrons to solid metal (hydr)oxides. Thus, multihaem c-Cyts play critical roles in S. oneidensis MR-1- and G. sulfurreducens-mediated dissimilatory reduction of solid metal (hydr)oxides by facilitating ET across the bacterial cell envelope.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                06 March 2019
                2019
                : 10
                : 464
                Affiliations
                [1] 1College of Materials and Energy, South China Agricultural University , Guangzhou, China
                [2] 2Guangdong Key Laboratory of Integrated Agro-Environmental Pollution Control and Management, Guangdong Institute of Eco-Environmental Science and Technology , Guangzhou, China
                Author notes

                Edited by: Fanghua Liu, Yantai Institute of Coastal Zone Research (CAS), China

                Reviewed by: Souichiro Kato, National Institute of Advanced Industrial Science and Technology (AIST), Japan; Liang Shi, China University of Geosciences, China

                *Correspondence: Tongxu Liu, txliu@ 123456soil.gd.cn

                These authors have contributed equally to this work

                This article was submitted to Microbiotechnology, Ecotoxicology and Bioremediation, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.00464
                6414795
                30894849
                860bf889-a34b-45b9-9156-8e5debfba33d
                Copyright © 2019 Liu, Wu, Liu, Li, Dong and Jing.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 26 September 2018
                : 21 February 2019
                Page count
                Figures: 8, Tables: 0, Equations: 0, References: 42, Pages: 10, Words: 0
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 41701305
                Award ID: 41522105
                Award ID: 21701045
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                extracellular electron transfer,temperature,redox transformation,mediator,biofilm

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