The Differing Roles of Flavins and Quinones in Extracellular Electron Transfer in Lactiplantibacillus plantarum

Tolar, Joe G.; Li, Siliang; Ajo‐Franklin, Caroline M.

doi:10.1128/aem.01313-22

Cited by 21 publications

(19 citation statements)

References 40 publications

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“…However, other genes in the FLEET locus were not induced, potentially indicating that those genes are dispensable for EET. To this regard, an L. plantarum mutant lacking the FLEET locus genes encoding electron transfer proteins EetA and EetB, or the heptaprenyl diphosphate synthase DmkB, was still able to perform DHNA-dependent EET, albeit at a somewhat reduced level compared to the wild-type strain (Tolar et al, 2022a). Instead, genes needed for anaerobic respiration, namely those coding for nitrate reductase ( narGHJI ) and the molybdopterin cofactor ( moeA, moeB ), were induced in mMRS with DHNA and FeAC ( Supplementary Table S2 ).…”

Section: Resultsmentioning

confidence: 99%

“…The L. plantarum EET pathway is present in other LAB and similar to the flavin-mediated FLEET system encoded by Listeria monocytogenes, a mainly respiratory Gram-positive species (Light et al, 2018; Rivera-Lugo et al, 2022). We found that L. plantarum NCIMB8826R requires ndh2, encoding a type-II NADH dehydrogenase, and conditionally requires pplA, predicted to encode a flavin-binding, membrane reductase, in the FLEET pathway to reduce extracellular ferric iron or a polarized anode (Tejedor-Sanz et al, 2022b; Tolar et al, 2022a).…”

Section: Introductionmentioning

confidence: 99%

“…However, L. plantarum lacks the other genes required for a complete menaquinone biosynthesis pathway (Watthanasakphuban et al, 2021). Instead, exogenous DHNA, a quinone present in foods and made by other bacteria, was sufficient for stimulating L. plantarum EET metabolism (Tejedor-Sanz et al, 2022b; Tolar et al, 2022a).…”

Section: Introductionmentioning

confidence: 99%

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Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Stevens

Beeck

Blackburn

et al. 2023

Preprint

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Extracellular electron transfer (EET) is a metabolic process that frequently uses quinones to couple intracellular redox reactions with extracellular electron acceptors. The physiological relevance of this metabolism for microorganisms that are capable of EET, but unable to synthesize their own quinones, remains to be determined. To address this question, we investigated quinone utilization by Lactiplantibacillus plantarum, a microorganism required for food fermentations, performs EET, and is also a quinone auxotroph. L. plantarum selectively used 1,4-dihydroxy-2-naphthoic acid (DHNA), 2-amino-3-carboxy-1,4-naphthoquinone (ACNQ), 1,4-naphthoquinone, and menadione for EET reduction of insoluble iron (ferrihydrite). However, those quinones used for EET also inhibited L. plantarum growth in non-aerated conditions. Transcriptomic analysis showed that DHNA induced oxidative stress in L. plantarum and this was alleviated by the inclusion of an electron acceptor, soluble ferric ammonium citrate (FeAC), in the laboratory culture medium. The presence of DHNA and FeAC during growth also induced L. plantarum EET metabolism, although activity was still dependent on the presence of exogenous electron shuttles. To determine whether quinone-producing bacteria frequently found together with L. plantarum in food fermentations could be a source of those electron shuttles, L. plantarum EET was measured after incubation with Lactococcus lactis and Leuconostoc mesenteroides. Quinone-producing L. lactis, but not a quinone-deficient L. lactis ΔmenC mutant, increased L. plantarum ferrihydrite reduction and medium acidification through an EET-dependent mechanism. L. plantarum EET was also stimulated by L. mesenteroides, and this resulted in greater environmental acidification and transient increases in L. plantarum growth. Overall, our findings revealed that L. plantarum overcomes the toxic effects of exogenous quinones to use those compounds, including those made by related bacteria, for EET-conferred, ecological advantages during the early stages of food fermentations.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Stevens

Beeck

Blackburn

et al. 2023

Preprint

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“…The direct electron donor(s) to ferric ion in the cell envelope of E. faecalis and other Gram-positive electrogenic bacteria, such as Listeria monocytogemes and Lactiplantibacillus plantarum , is not known. It might be electron-conductive pili, one or more flavoproteins exposed on the outer side of the cytoplasmic membrane, and depend on small soluble redox compounds in the cell envelope [ 26 , 37 , 39 ]. The so-far-reported screens for ferric reductase-defective mutants of L. monocytogenes and E. faecalis based on colony Ferrozine zymogram staining have not identified any genes outside of the so called FLEET locus, comprising pplA , eetAB , and ndh2/3 , and dmkAB genes for quinone synthesis [ 14 , 27 ] (this work).…”

Section: Discussionmentioning

confidence: 99%

Enterococcus faecalis NADH Peroxidase-Defective Mutants Stain Falsely in Colony Zymogram Assay for Extracellular Electron Transfer to Ferric Ions

Hederstedt

2022

Microorganisms

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Enterococcus faecalis cells can reduce ferric ions and other electron acceptors by extracellular electron transfer (EET). To find mutants with enhanced or defective EET, strain OG1RF with random transposon insertions in the chromosome was screened for ferric reductase activity by colony zymogram staining using the chromogenic ferrous-chelating compound Ferrozine. The screen revealed npr, eetB, and ndh3 mutants. The aberrant ferric reductase phenotype of Npr (NADH peroxidase)-defective mutants was found to be a property of colonies and not apparent with washed cells grown in liquid culture. EetB- and Ndh3-defective mutants, in contrast, consistently showed low ferric reductase activity. It is concluded that colony zymogram staining for ferric reductase activity using Ferrozine can be misleading, especially through false negative results. It is suggested that hydrogen peroxide produced in the colony quenches the zymogram staining. In addition, it is demonstrated that the negative effect of heme on EET to ferric ion in E. faecalis is relieved by cytochrome bd deficiency. The findings can help to identify bacteria with EET ability and contribute to our understanding of EET in Gram-positive bacteria and the physiology of E. faecalis.

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“…Within this cluster, we found that the fmnB gene encoded an ApbE-like protein that flavinylated a second protein from the cluster, PplA, at two sites ( 11 , 12 ). Homologous genes are present in a number of related members of the Firmicutes and have been implicated in similar EET activities in several bacteria ( 13 – 17 ). We further found that FmnB is essential for the flavinylation of the extracytosolic fumarate reductase FrdA, a flavin reductase encoded outside the EET gene cluster that uses fumarate as an electron acceptor ( 18 ).…”

Section: Introductionmentioning

confidence: 99%

Distinct Energy-Coupling Factor Transporter Subunits Enable Flavin Acquisition and Extracytosolic Trafficking for Extracellular Electron Transfer in Listeria monocytogenes

Rivera‐Lugo

Huang

Lee

et al. 2023

mBio

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Bacteria import vitamins and other essential compounds from their surroundings but also traffic related compounds from the cytosol to the cell envelope where they serve various functions. Studying the foodborne pathogen Listeria monocytogenes , we find that the modular use of subunits from a prominent class of bacterial transporters enables the import of environmental vitamin B 2 cofactors and the extracytosolic trafficking of a vitamin B 2 -derived cofactor that facilitates redox reactions in the cell envelope.

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The Differing Roles of Flavins and Quinones in Extracellular Electron Transfer in Lactiplantibacillus plantarum

Cited by 21 publications

References 40 publications

Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Lactiplantibacillus plantarumuses ecologically relevant, exogenous quinones for extracellular electron transfer

Enterococcus faecalis NADH Peroxidase-Defective Mutants Stain Falsely in Colony Zymogram Assay for Extracellular Electron Transfer to Ferric Ions

Distinct Energy-Coupling Factor Transporter Subunits Enable Flavin Acquisition and Extracytosolic Trafficking for Extracellular Electron Transfer in Listeria monocytogenes

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