Two Modes of Riboflavin-Mediated Extracellular Electron Transfer in Geobacter uraniireducens

Huang, Lingyan; Tang, Jiahuan; Chen, Man; Liu, Xing; Zhou, Shungui

doi:10.3389/fmicb.2018.02886

Cited by 65 publications

(34 citation statements)

References 31 publications

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“…Geobacter species can use different mechanisms for metal ion reduction and for current generation. In addition, it has been shown that an efficient Fe(III) oxide reduction did not mean the same efficient current generation in Geobacter species and vice versa (Huang et al, ; Rotaru et al, ; Tan et al, ). In particular, G. sulfurreducens used different ways to respire Fe(III) oxide and anode.…”

Section: Discussionmentioning

confidence: 99%

“…Fe(III) reduction could have been an important process on early Earth that drives microbial evolution. In particular, Geobacter species have evolved different ways to respire Fe(III) oxides over billions of years (Holmes et al, ; Huang et al, ). Even under laboratory conditions, Geobacter species have shown adaptive evolution to efficiently reduce Fe(III) oxides (Smith et al, ; Summers et al, ; Tremblay et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Thus, it can be speculated that Fe(III) minerals may act as positive selective pressures to drive the evolution of Geobacter species (Smith et al, ). In fact, over billions of years, Geobacter species have evolved different ways to respire insoluble Fe(III) oxides (Huang, Tang, Chen, Liu, & Zhou, ; Reguera et al, ; Tan et al, ). Considering the requirement of e‐pili for efficient extracellular respiration by G. sulfurreducens , we hypothesize that truncation of the full‐length ancestral PilA arises from adaptive evolution to confer the ability to respire Fe(III) oxides in the evolutionary history of G. sulfurreducens .…”

Section: Introductionmentioning

confidence: 99%

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Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Liu

Yin

Xiao

et al. 2019

Molecular Microbiology

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The electrically conductive pili (e-pili) of Geobacter species enable extracellular electron transfer to insoluble metallic minerals, electrodes and other microbial species, which confers biogeochemical significance and global prevalence on Geobacter in diverse anaerobic environments. E-pili are constructed by truncated PilA which is considered to have evolved from full-length pilin by gene fission under positive evolutionary selection. However, this hypothesis is based on phylogenetic analysis and has not yet been experimentally confirmed. Here, we reconstructed an ancestral strain of G. sulfurreducens (designated COMB) carrying full-length PilA by combining genes GSU1496 and GSU1497. The results demonstrated that strain COMB expressed and assembled the full-length fused PilA and exhibited an outer membrane c-type cytochrome profile similar to the wild-type strain. Surprisingly, the generated COMB-pili were also conductive, indicating the evolution of truncated PilA did not occur for conductivity. Moreover, strain COMB minimally reduced Fe(III) oxides but maintained its ability to respire electrodes, demonstrating the truncation of pilin enables iron respiration. This study provides the first experimental evidence that the truncation of pilin in Geobacter species confers adaption to Fe(III)-mineral-mediated selective pressures, and suggests an evolutionary event during which the separation of the GSU1497 gene helped Geobacter survive and thrive in natural environments. K E Y W O R D S adaptive evolution, dissimilatory iron reduction, e-pili, Geobacter sulfurreducens, truncated pilin S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Liu X, Ye Y, Xiao K, Rensing C, Zhou S. Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments. Mol Microbiol. 2020;113:783-793.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Liu

Yin

Xiao

et al. 2019

Molecular Microbiology

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“…They can transfer electrons to the mineral surface by direct contact or by using flavins [e.g., flavin mononucleotide (FMN) and riboflavin] as extracellular electron shuttles (von Canstein et al, 2008; Shi et al, 2016). The latter approach has been shown to be faster for reduction of Fe(III) (hydr)oxides (von Canstein et al, 2008; Ross et al, 2009; Huang et al, 2018). FMN and riboflavin as extracellular electron shuttles can be secreted by many bacteria (such as Shewanella oneidensis strain MR-1, Shewanella decolorationis strain S12, and Geobacter sulfurreducens ) (von Canstein et al, 2008; Kotloski and Gralnick, 2013; Okamoto et al, 2014; Yang et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Effects of Flavin-Goethite Interaction on Goethite Reduction by Shewanella decolorationis S12

Zhao

et al. 2019

Front. Microbiol.

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Flavin mononucleotide (FMN) and riboflavin are structurally similar flavins, except for the presence of a phosphate group on the FMN molecule. They are used by a variety of electroactive bacteria as extracellular electron shuttles in microbial Fe reduction and inevitably interact with Fe (hydr)oxides in the extracellular environment. It is currently unknown whether flavin/Fe (hydr)oxide interaction interferes with extracellular electron transfer (EET) to the mineral surface. In this study, we found that the goethite reduction rate was lower when mediated by FMN than by RF, suggesting that FMN was less effective in shuttling electrons between cells and minerals. Nevertheless, the phosphate group did not prevent the FMN molecule from accepting electrons from bacterial cells and transferring electrons to the mineral. Results of adsorption experiment, attenuated total reflectance (ATR) Fourier transform infrared (FTIR) spectroscopy, and bacterial attachment trend analyses showed that FMN exhibited strong adsorption on goethite surface by forming phosphate inner-sphere complex, which prevented bacterial cells from approaching goethite. Therefore, the interaction between FMN and goethite surface may increase the distance of electron transfer from bacterial cells to goethite and result in lower EET efficiency in comparison to those mediated by riboflavin. To our knowledge, these data reveal for the first time that the interaction between flavin and Fe (hydr)oxide affect flavin-mediated electron transfer to mineral surface and add a new dimension to our understanding of flavin-mediated microbial Fe reduction processes.

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“…The debate on the composition of nanowires and their role in long-range electron transfer continues. Moreover, self-secreted flavins contribute to Geobacter EET as cofactors by binding to outer membrane c -Cyts when electrodes are used as electron acceptors ( Okamoto et al, 2014a ; Okamoto et al, 2014b ; Huang et al, 2018 ; Thirumurthy and Jones, 2020 ). Based on these studies, two microbial EET pathways have been proposed: direct EET via c -Cyts or electrically conductive nanowires and indirect EET via exogenous or endogenous electron shuttles.…”

Section: Extracellular Electron Transfer Of Geobacter and Shewanella : Biofilm Vs Planktonic Exoelementioning

confidence: 99%

Biofilm Biology and Engineering of Geobacter and Shewanella spp. for Energy Applications

Wang

Han

et al. 2021

Front. Bioeng. Biotechnol.

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Geobacter and Shewanella spp. were discovered in late 1980s as dissimilatory metal-reducing microorganisms that can transfer electrons from cytoplasmic respiratory oxidation reactions to external metal-containing minerals. In addition to mineral-based electron acceptors, Geobacter and Shewanella spp. also can transfer electrons to electrodes. The microorganisms that have abilities to transfer electrons to electrodes are known as exoelectrogens. Because of their remarkable abilities of electron transfer, Geobacter and Shewanella spp. have been the two most well studied groups of exoelectrogens. They are widely used in bioelectrochemical systems (BESs) for various biotechnological applications, such as bioelectricity generation via microbial fuel cells. These applications mostly associate with Geobacter and Shewanella biofilms grown on the surfaces of electrodes. Geobacter and Shewanella biofilms are electrically conductive, which is conferred by matrix-associated electroactive components such as c-type cytochromes and electrically conductive nanowires. The thickness and electroactivity of Geobacter and Shewanella biofilms have a significant impact on electron transfer efficiency in BESs. In this review, we first briefly discuss the roles of planktonic and biofilm-forming Geobacter and Shewanella cells in BESs, and then review biofilm biology with the focus on biofilm development, biofilm matrix, heterogeneity in biofilm and signaling regulatory systems mediating formation of Geobacter and Shewanella biofilms. Finally, we discuss strategies of Geobacter and Shewanella biofilm engineering for improving electron transfer efficiency to obtain enhanced BES performance.

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Two Modes of Riboflavin-Mediated Extracellular Electron Transfer in Geobacter uraniireducens

Cited by 65 publications

References 31 publications

Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Molecular evidence for the adaptive evolution of Geobacter sulfurreducens to perform dissimilatory iron reduction in natural environments

Effects of Flavin-Goethite Interaction on Goethite Reduction by Shewanella decolorationis S12

Biofilm Biology and Engineering of Geobacter and Shewanella spp. for Energy Applications

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