Identification of an ECF sigma factor that facilitates electroactive biofilm formation by Shewanella oneidensis MR-1
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ABSTRACT:
ORGANISM(S): Shewanella oneidensis MR-1 Shewanella oneidensis
PROVIDER: GSE142643 | GEO | 2020/06/01
REPOSITORIES: GEO
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Project description:Shewanella oneidensis MR-1 was grown on electrodes in electrochemical flow cells (EFC), and the transcriptome profiles of electrode-attached MR-1 cells were compared under electrolyte-flow and static (non-flow) conditions. The results revealed that the SO_3096 gene encoding a putative extracytoplasmic function (ECF) sigma factor, as well as genes related to cyclic-di-guanosine monophosphate and flagella synthesis (e.g., SO_3556 and flrC) and c-type cytochrome maturation (dsbD), was significantly up-regulated under the electrolyte-flow condition. Compared to wild-type MR-1 (WT), a deletion mutant of SO_3096 (∆SO_3096) showed an impaired biofilm formation and a decreased current generation in EFC, suggesting that the ECF sigma factor encoded by this gene is involved in the regulation of biofilm formation and current generation under electrolyte-flow conditions. We also compared the transcriptome profiles of WT and ∆SO_3096 grown in EFC, confirming that many genes up-regulated under the electrolyte-flow condition, including dsbD, were down-regulated in ∆SO_3096. Transcription analysis using lacZ as a reporter gene showed that the promoter of dsbD is activated in the presence of SO_3096. Measurement of current generation by a dsbD-deletion mutant revealed that this gene is essential for electron transfer to electrodes. These results suggest that the SO_3096 protein serves as an ECF sigma factor that regulates cellular functions related to electroactive biofilm formation under electrolyte-flow conditions.
2020-06-01 | GSE142642 | GEO
Project description:Shewanella oneidensis MR-1 was grown on electrodes in electrochemical flow cells (EFC), and the transcriptome profiles of electrode-attached MR-1 cells were compared under electrolyte-flow and static (non-flow) conditions. The results revealed that the SO_3096 gene encoding a putative extracytoplasmic function (ECF) sigma factor, as well as genes related to cyclic-di-guanosine monophosphate and flagella synthesis (e.g., SO_3556 and flrC) and c-type cytochrome maturation (dsbD), was significantly up-regulated under the electrolyte-flow condition. Compared to wild-type MR-1 (WT), a deletion mutant of SO_3096 (∆SO_3096) showed an impaired biofilm formation and a decreased current generation in EFC, suggesting that the ECF sigma factor encoded by this gene is involved in the regulation of biofilm formation and current generation under electrolyte-flow conditions. We also compared the transcriptome profiles of WT and ∆SO_3096 grown in EFC, confirming that many genes up-regulated under the electrolyte-flow condition, including dsbD, were down-regulated in ∆SO_3096. Transcription analysis using lacZ as a reporter gene showed that the promoter of dsbD is activated in the presence of SO_3096. Measurement of current generation by a dsbD-deletion mutant revealed that this gene is essential for electron transfer to electrodes. These results suggest that the SO_3096 protein serves as an ECF sigma factor that regulates cellular functions related to electroactive biofilm formation under electrolyte-flow conditions.
2020-06-01 | GSE142641 | GEO
Project description:In many bacteria, cyclic diguanosine monophosphate (c-di-GMP), synthesized by diguanylate cyclase (DGC), serves as a second messenger involved in the regulation of biofilm formation. Although studies have suggested that c-di-GMP also regulates the formation of electrochemically active biofilms (EABFs) by Shewanella oneidensis MR-1, DGCs involved in this process remained to be identified. Here, we report that the SO_1646 gene, hereafter named dgcS, is upregulated under medium flow conditions in electrochemical flow cells (EFCs), and its product (DgcS) functions as a major DGC in MR-1. In vitro assays demonstrated that purified DgcS catalyzed the synthesis of c-di-GMP from GTP. Comparisons of intracellular c-di-GMP levels in the wild-type strain and a dgcS deletion mutant (ΔdgcS mutant) showed that production of c-di-GMP was markedly reduced in the ΔdgcS mutant when cells were grown in batch cultures and on electrodes in EFCs. Cultivation of the ΔdgcS mutant in EFCs also revealed that the loss of DgcS resulted in impaired biofilm formation and decreased current generation. These findings demonstrate that MR-1 uses DgcS to synthesize c-di-GMP under medium flow conditions, thereby activating biofilm formation on electrodes.IMPORTANCE Bioelectrochemical systems (BESs) have attracted wide attention owing to their utility in sustainable biotechnology processes, such as microbial fuel cells and electrofermentation systems. In BESs, electrochemically active bacteria (EAB) form biofilms on electrode surfaces, thereby serving as effective catalysts for the interconversion between chemical and electric energy. It is therefore important to understand mechanisms for the formation of biofilm by EAB grown on electrodes. Here, we show that a model EAB, S. oneidensis MR-1, expresses DgcS as a major DGC, thereby activating the formation of biofilms on electrodes via c-di-GMP-dependent signal transduction cascades. The findings presented herein provide the molecular basis for improving electrochemical interactions between EAB and electrodes in BESs. The results also offer molecular insights into how Shewanella regulates biofilm formation on solid surfaces in the natural environment.
| S-EPMC8091010 | biostudies-literature
Project description:Identification of an ECF sigma factor that facilitates electroactive biofilm formation by Shewanella oneidensis MR-1
| PRJNA597846 | ENA
Project description:Shewanella oneidensis MR-1 is capable of forming highly structured surface-attached communities. By DNase I treatment, we demonstrated that extracellular DNA (eDNA) serves as a structural component in all stages of biofilm formation under static and hydrodynamic conditions. We determined whether eDNA is released through cell lysis mediated by the three prophages LambdaSo, MuSo1 and MuSo2 that are harbored in the genome of S. oneidensis MR-1. Mutant analyses and infection studies revealed that all three prophages may individually lead to cell lysis. However, only LambdaSo and MuSo2 form infectious phage particles. Phage release and cell lysis already occur during early stages of static incubation. A mutant devoid of the prophages was significantly less prone to lysis in pure culture. In addition, the phage-less mutant was severely impaired in biofilm formation through all stages of development, and three-dimensional growth occurred independently of eDNA as a structural component. Thus, we suggest that in S. oneidensis MR-1 prophage-mediated lysis results in the release of crucial biofilm-promoting factors, in particular eDNA.
| S-EPMC3105746 | biostudies-literature
Project description:Identification of an ECF sigma factor that facilitates electroactive biofilm formation by Shewanella oneidensis MR-1: Experiment 2
| PRJNA597849 | ENA
Project description:Identification of an ECF sigma factor that facilitates electroactive biofilm formation by Shewanella oneidensis MR-1: Experiment 1
| PRJNA597850 | ENA
Project description:Microbial electrochemical technologies (METs) have emerged in recent years as a promising alternative green source of energy, with microbes consuming organic matter to produce energy or valuable byproducts. It is the ability of performing extracellular electron transfer that allows these microbes to exchange electrons with an electrode in these systems. The low levels of current achieved have been the limiting factor for the large-scale application of METs. Shewanella oneidensis MR-1 is one of the most studied electroactive organisms regarding extracellular electron transfer, and it has been shown that biofilm formation is a key factor for current generation. The transcription factor bolA has been identified as a central player in biofilm formation in other organisms, with its overexpression leading to increased biofilm. In this work we explore the effect of this gene in biofilm formation and current production by S. oneidensis MR-1. Our results demonstrate that an increased biofilm formation and consequent current generation was achieved by the overexpression of this gene. This information is crucial to optimize electroactive organisms toward their practical application in METs.
| S-EPMC7225295 | biostudies-literature
Project description:Although microbial activity and associated iron (oxy)hydroxides are known in general to affect the environmental dynamics of 4-hydroxy-3-nitrobenzenearsonic acid (roxarsone), the mechanistic understanding of the underlying biophysico-chemical processes remains unclear due to limited experimental information. We studied how Shewanella oneidensis MR-1 -a widely distributed metal-reducing bacterium, in the presence of dissolved Fe(III), affects roxarsone transformations and biogeochemical cycling in a model aqueous system. The results showed that the MR-1 strain was able to anaerobically use roxarsone as a terminal electron acceptor and to convert it to a single product, 3-amino-4-hydroxybenzene arsonic acid (AHBAA). The presence of Fe(III) stimulated roxarsone transformation via MR-1-induced Fe(III) reduction, whereby the resulting Fe(II) acted as an efficient reductant for roxarsone transformation. In addition, the subsequent secondary Fe(III)/Fe(II) mineralization created conditions for adsorption of organoarsenic compounds to the yielded precipitates and thereby led to arsenic immobilization. The study provided direct evidence of Shewanella oneidensis MR-1-induced direct and Fe(II)-associated roxarsone transformation. Quantitative estimations revealed a candidate mechanism for the early-stage environmental dynamics of roxarsone in nature, which is essential for understanding the environmental dynamics of roxarsone and successful risk assessment.
| S-EPMC4839622 | biostudies-literature
Project description:BackgroundSome microorganisms can respire with extracellular electron acceptors using an extended electron transport chain to the cell surface. This process can be applied in bioelectrochemical systems in which the organisms produce an electrical current by respiring with an anode as electron acceptor. These organisms apply flavin molecules as cofactors to facilitate one-electron transfer catalyzed by the terminal reductases and in some cases as endogenous electron shuttles.ResultsIn the model organism Shewanella oneidensis, riboflavin production and excretion trigger a specific biofilm formation response that is initiated at a specific threshold concentration, similar to canonical quorum-sensing molecules. Riboflavin-mediated messaging is based on the overexpression of the gene encoding the putrescine decarboxylase speC which leads to posttranscriptional overproduction of proteins involved in biofilm formation. Using a model of growth-dependent riboflavin production under batch and biofilm growth conditions, the number of cells necessary to produce the threshold concentration per time was deduced. Furthermore, our results indicate that specific retention of riboflavin in the biofilm matrix leads to localized concentrations, which by far exceed the necessary threshold value.ConclusionThis study describes a new quorum-sensing mechanism in S. oneidensis. Biofilm formation of S. oneidensis is induced by low concentrations of riboflavin resulting in an upregulation of the ornithine-decarboxylase speC. The results can be applied for the development of strains catalyzing increased current densities in bioelectrochemical systems.
| S-EPMC8176591 | biostudies-literature