Fumarate disproportionation by Geobacter sulfurreducens and its involvement in biocorrosion and interspecies electron transfer

Shi, Xiaochen; Tremblay, Pier‐Luc; Xue, Meilan; Song, Xinyi; Zhang, Tian

doi:10.1016/j.scitotenv.2022.154251

Cited by 7 publications

(3 citation statements)

References 64 publications

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“…For coculture experiments with Geobacter species, G. metallireducens strains and G. sulfurreducens were grown with ethanol (20 mM) provided as the electron donor and fumarate (45 mM) as the electron acceptor in a freshwater medium as previously described 5 . Although G. sulfurreducens can disproportionate fumarate 56 , previous studies have demonstrated that fumarate is not disproportionated in G. metallireducens / G. sulfurreducens DIET cocultures 6 . Furthermore, we monitored ethanol oxidation by the coculture to ensure that growth was not due to fumarate disproportionation.…”

Section: Methodsmentioning

confidence: 99%

Different outer membrane c‐type cytochromes are involved in direct interspecies electron transfer to Geobacter or Methanosarcina species

Holmes

Zhou

Smith

et al. 2022

mLife

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Direct interspecies electron transfer (DIET) may be most important in methanogenic environments, but mechanistic studies of DIET to date have primarily focused on cocultures in which fumarate was the terminal electron acceptor. To better understand DIET with methanogens, the transcriptome of Geobacter metallireducens during DIET‐based growth with G. sulfurreducens reducing fumarate was compared with G. metallireducens grown in coculture with diverse Methanosarcina. The transcriptome of G. metallireducens cocultured with G. sulfurreducens was significantly different from those with Methanosarcina. Furthermore, the transcriptome of G. metallireducens grown with Methanosarcina barkeri, which lacks outer‐surface c‐type cytochromes, differed from those of G. metallireducens cocultured with M. acetivorans or M. subterranea, which have an outer‐surface c‐type cytochrome that serves as an electrical connect for DIET. Differences in G. metallireducens expression patterns for genes involved in extracellular electron transfer were particularly notable. Cocultures with c‐type cytochrome deletion mutant strains, ∆Gmet_0930, ∆Gmet_0557 and ∆Gmet_2896, never became established with G. sulfurreducens but adapted to grow with all three Methanosarcina. Two porin–cytochrome complexes, PccF and PccG, were important for DIET; however, PccG was more important for growth with Methanosarcina. Unlike cocultures with G. sulfurreducens and M. acetivorans, electrically conductive pili were not needed for growth with M. barkeri. Shewanella oneidensis, another electroactive microbe with abundant outer‐surface c‐type cytochromes, did not grow via DIET. The results demonstrate that the presence of outer‐surface c‐type cytochromes does not necessarily confer the capacity for DIET and emphasize the impact of the electron‐accepting partner on the physiology of the electron‐donating DIET partner.

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Section: Methodsmentioning

confidence: 99%

Different outer membrane c‐type cytochromes are involved in direct interspecies electron transfer to Geobacter or Methanosarcina species

Holmes

Zhou

Smith

et al. 2022

mLife

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“…This was recently illustrated through its disproportionation by an evolved strain of the electroactive bacteria Geobacter sulfurreducens which was able to utilise a fraction of the fumarate as an electron donor and a fraction as electron acceptor. 40 While it is unknown if this was also occurring in the mixed-species community of the present study, it highlights the multifaceted considerations of soluble alternatives to the electrode.…”

Section: Resultsmentioning

confidence: 79%

Extracellular Electron Transfer of Weak Electricigens in the Presence of a Competing Electron Acceptor

Aiyer

Doyle

2023

J. Electrochem. Soc.

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To maximise microbial electroactivity in bioelectrochemical systems, soluble electron acceptors are typically omitted as they compete with the electrode. While practical, this approach provides engineered conditions that do not reflect the natural environment of electroactive microorganisms, which may contain both soluble and insoluble electron acceptors. This study investigates the behaviour of weak electricigens, a relatively understudied category of microorganisms whose members switch between non-electroactive and electroactive states. Enrichments were performed in microbial fuel cells (MFCs) containing both an electrode and the soluble alternative fumarate to probe extracellular electron transfer of weak electricigens. Using fluorescence spectroscopy, chromatography and voltammetry, the electron shuttle riboflavin was not found in these conditions but was found in controls in which only the electrode is available to reduce. Despite this dichotomy in ability to perform riboflavin-based mediated electron transfer, communities of weak electricigens were similarly electroactive in each condition (19.36 ± 0.9 mW m-2 versus 20.25 ± 2.0 mW m-2). 16S rRNA gene sequencing revealed similar communities enriched in each condition, but with differing abundance. Understanding EET in natural environments is of both fundamental and applied interest, as it can inform the design of real-world bioelectrochemical systems whose influents are likely to contain competing electron acceptors.

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“…Supplementary Figure S1 shows metabolisms of ethanol, fumarate, malate and succinate between these Geobacte r species during co-culture. The chemical compounds were separated with an Aminex NPX-87H column (Bio-Rad Laboratories, Shanghai, China) ( Summers et al, 2010 ; Shi et al, 2022 ). Ethanol, malate and succinate were purchased from Sinopharm Chemical Reagent Co., Ltd. Quantitative PCR (qPCR) was used to monitor bacterial growth during co-culture (QuantStudio3, Thermo Fisher Scientific China Co., Ltd., Shanghai, China) ( Summers et al, 2010 ).…”

Section: Methodsmentioning

confidence: 99%

The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens

Jiang,

He,

Luo

et al. 2023

Front. Microbiol.

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Geobacter sulfurreducens mediates extracellular electron transfer (EET) reactions with different substrates, such as solid-phase Fe(III)-containing minerals, anodes and the cells of Geobacter metallireducens. To compare their roles in EET, the pilA-N, omcE, omcS, omcT and omcZ genes of G. sulfurreducens were systematically deleted. All mutants showed impaired and varied ability to form biofilms on nonconductive surface. Deletion of omcE also impaired bacterial ability to reduce ferrihydrite, but its impacts on the ability for anode reduction and the co-culture of G. metallireducens-G. sulfurreducens were minimal. The mutant without omcS showed diminished ability to reduce ferrihydrite and to form the co-culture, but was able to regain its ability to reduce anodes. Deletion of omcT, omcZ or pilA-N alone impaired bacterial ability to reduce ferrihydrite and anodes and to form the co-culture. Deletion of all tested genes abolished bacterial ability to reduce ferrihydrite and anodes. Triple-deletion of all omcS, omcT and omcZ abolished the ability of G. sulfurreducens to co-culture with G. metallireducens. However, deletion of only omcZ or pilA-N or both omcS and omcT abolished the ability of G. sulfurreducens without hydrogenase gene hybL to co-culture with G. metallireducens, which show their indispensable roles in direct electron transfer from G. metallireducens to G. sulfurreducens. Thus, the roles of pilA-N, omcE, omcS, omcT and omcZ for G. sulfurreducens in EET vary substantially, which also suggest that possession of PilA-N and multiple cytochromes of different structures enables G. sulfurreducens to mediate EET reactions efficiently with substrates of different properties.

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Fumarate disproportionation by Geobacter sulfurreducens and its involvement in biocorrosion and interspecies electron transfer

Cited by 7 publications

References 64 publications

Different outer membrane c‐type cytochromes are involved in direct interspecies electron transfer to Geobacter or Methanosarcina species

Different outer membrane c‐type cytochromes are involved in direct interspecies electron transfer to Geobacter or Methanosarcina species

Extracellular Electron Transfer of Weak Electricigens in the Presence of a Competing Electron Acceptor

The varied roles of pilA-N, omcE, omcS, omcT, and omcZ in extracellular electron transfer by Geobacter sulfurreducens

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