A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria

Abstract

Extracellular electron transfer (EET) describes microbial bioelectrochemical processes in which electrons are transferred from the cytosol to the exterior of the cell1. Mineral-respiring bacteria use elaborate haem-based electron transfer mechanisms2,3,4 but the existence and mechanistic basis of other EETs remain largely unknown. Here we show that the food-borne pathogen Listeria monocytogenes uses a distinctive flavin-based EET mechanism to deliver electrons to iron or an electrode. By performing a forward genetic screen to identify L. monocytogenes mutants with diminished extracellular ferric iron reductase activity, we identified an eight-gene locus that is responsible for EET. This locus encodes a specialized NADH dehydrogenase that segregates EET from aerobic respiration by channelling electrons to a discrete membrane-localized quinone pool. Other proteins facilitate the assembly of an abundant extracellular flavoprotein that, in conjunction with free-molecule flavin shuttles, mediates electron transfer to extracellular acceptors. This system thus establishes a simple electron conduit that is compatible with the single-membrane structure of the Gram-positive cell. Activation of EET supports growth on non-fermentable carbon sources, and an EET mutant exhibited a competitive defect within the mouse gastrointestinal tract. Orthologues of the genes responsible for EET are present in hundreds of species across the Firmicutes phylum, including multiple pathogens and commensal members of the intestinal microbiota, and correlate with EET activity in assayed strains. These findings suggest a greater prevalence of EET-based growth capabilities and establish a previously underappreciated relevance for electrogenic bacteria across diverse environments, including host-associated microbial communities and infectious disease.

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Fig. 1: An uncharacterized genetic locus associated with EET activity.
Fig. 2: A parallel electron transfer pathway segregates EET from aerobic respiration.
Fig. 3: A surface-associated flavoprotein establishes the extracellular component of the EET apparatus.
Fig. 4: EET supports anaerobic growth, confers a competitive advantage in the intestinal lumen, and is active in multiple Firmicutes.

Data availability

The datasets generated during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank G. Chen, J.-D. Sauer, E. Stevens, M. Marco and N. Freitag for providing bacterial strains; H. Carlson, A. Williamson and J. Coates for helpful feedback; and N. Garelis for experimental assistance. Research reported in this publication was supported by funding from the National Institute of Allergy and Infectious Diseases of the National Institutes of Health (F32AI136389 to S.H.L., 1P01 AI063302 to D.A.P., and 1R01 AI27655 to D.A.P.), the Office of Naval Research (N0001417WX01603 to C.M.A.-F.), and the China Scholarship Council (no. 201606090098 to L.S.). A mass spectrometer used in this study was purchased with NIH support (grant 1S10OD020062-01). Work at the Molecular Foundry was supported by the Office of Science, Office of Basic Energy Sciences, of the US Department of Energy under Contract No. DE-AC02-05CH11231.

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Nature thanks N. Freitag, J. Gralnick, K. Nealson and G. Reguera for their contribution to the peer review of this work.

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S.H.L., A.T.I., C.M.A.-F. and D.A.P. designed the study. S.H.L, L.S. and J.A.C. performed electrochemical experiments. S.H.L. and A.T.I. performed mass spectrometric experiments. S.H.L., A.L. and R.R.-L. performed microbiological and biochemical experiments. S.H.L. and D.A.P. wrote the manuscript.

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Correspondence to Daniel A. Portnoy.

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D.A.P. has a consulting relationship with and a financial interest in Aduro Biotech; both he and the company stand to benefit from the commercialization of this research.

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Extended data figures and tables

Extended Data Fig. 1 Electrochemical analyses of L. monocytogenes.

a, The double chamber cell used for electrochemical experiments. CE, counter electrode; CEM, cation exchange membrane; RE, reference electrode; WE, working electrode. Inlets and outlets for N2 gas are labelled. b, Cyclic voltammograms of wild-type and ndh2::tn strains of L. monocytogenes. ‘Abiotic’ refers to an uninoculated control. Arrows highlight the initiation of the catalytic wave. Results are representative of three independent experiments. Source data

Extended Data Fig. 2 EET activity maintains cellular redox homeostasis.

Ratio of NAD+ to NADH in wild-type and ndh2::tn strains supplemented with ferric ammonium citrate under aerobic or microaerophilic conditions. Results from three independent experiments are expressed as mean ± s.e.m. A statistically significant difference between microaerophilic cells incubated with or without iron is indicated; *P = 0.0015, unpaired two-sided t-test. Source data

Extended Data Fig. 3 Evidence that a distinct menaquinone derivative functions in aerobic respiration.

a, Ferric iron reductase activity of mutants described in Fig. 2 demonstrates that genes essential for growth on aerobic respiration medium are dispensable for EET. Results from three independent experiments are expressed as mean ± s.e.m. b, The L. monocytogenes hep operon. Notably, menG—which encodes demethylmenaquinone transferase (the enzyme that converts demethylmenaquinone to menaquione) (Fig. 2b)—neighbours the hepT and hepS genes, which function in quinone biosynthesis and are essential for aerobic respiration (Fig. 2c). Source data

Extended Data Fig. 4 Recombinant FmnB FMNylates PplA at two discrete sites.

a, b, Deconvoluted mass spectra from a single experiment of recombinant PplA (a) and recombinant PplA incubated with FAD + FmnB (b). The observed molecular weight change (877 Da) is consistent with two post-translational FMNylations (2 × 438.3 Da) on PplA. Source data

Extended Data Fig. 5 Proposed role of RibU and FmnA in FAD secretion.

a, Simplified adaptation of a previously proposed model of L. monocytogenes riboflavin uptake through the RibU, EcfT, EcfA and EcfA’ transporter10. According to this model, EcfT, EcfA and EcfA’ couple ATP hydrolysis with conformational changes that result in substrate bound to RibU being released into the cytosol. b, On the basis of protein homology (FmnA shares 50% sequence identity with EcfT) and the expectation that extracellular FAD is required for FmnB to catalyse FMNylation of PplA, we propose that the FmnA interacts with RibU to promote FAD secretion. c, Ferric iron reductase activity of strains incubated with 0.5 mM FAD for 1 h. The ability of exogenous FAD to specifically rescue ferric iron reductase activity in the fmnA::tn and ribU::tn strains is consistent with FmnA and RibU functioning in FAD secretion. Results from three independent experiments are expressed as mean ± s.e.m. Statistically significant differences between untreated and FAD-treated cells are indicated; *P = 0.038, **P < 0.0001, unpaired two-sided t-test. Source data

Extended Data Fig. 6 Flavin shuttles promote EET activity.

a, Chronoamperometry results from L. monocytogenes-inoculated electrochemical reactors with 1 μM FMN injections at the indicated time points. Results are representative of three independent experiments. b, The effect of flavins on L. monocytogenes (Lm) ferric iron reductase activity with insoluble ferric (hydr)oxide (top) and soluble ferric ammonium citrate (bottom). With insoluble substrate the local iron concentration for most cells is low, whereas with soluble substrate the concentration of iron in the direct vicinity of cells is high (insets). Results from three independent experiments are expressed as mean ± s.e.m. Source data

Extended Data Fig. 7 EET supports anaerobic growth on ferric iron.

a, Growth following incubation of L. monocytogenes strains on xylitol medium without (left) or with (right) ferric iron under aerobic (top) or anaerobic (bottom) conditions. Results are representative of three independent experiments. Strain labels are coloured based on attributed deficiencies (Fig. 2d) in aerobic respiration (blue) or EET (red). Ndh1 and Ndh2 are probably functionally redundant under aerobic conditions, as a growth phenotype is only observed in the double mutant. Note the visual evidence of ferrous iron production in the agar adjoining anaerobically growing cells. b, CFUs of L. monocytogenes strains anaerobically incubated in xylitol medium without (−) or with (+) ferric supplementation. Results for soluble ferric ammonium citrate (top) and insoluble ferric (hydr)oxide (bottom) are shown. Dashed lines denote the number of cells at the start of the experiment. Results from three independent experiments are expressed as mean ± s.e.m. Statistically significant differences in the ferric iron-supplemented condition are noted; ***P < 0.0001, unpaired two-sided t-test. Source data

Extended Data Fig. 8 EET genes are dispensable for L. monocytogenes intracellular growth.

a, Mouse bone-marrow-derived macrophages were infected with L. monocytogenes, and CFUs were enumerated at the indicated times. Results from three independent experiments are expressed as mean ± s.e.m. b, L. monocytogenes burdens in mouse organs (n = 5) 48 h after intravenous infection. Representative results from two independent experiments are expressed as median and s.e. Source data

Extended Data Fig. 9 Identified EET loci are widespread in the Firmicutes phylum.

a, Phylogenetic tree constructed from select Ndh2 homologue sequences. A more comprehensive list of organisms that possess an EET locus is provided in Supplementary Table 3. Labels on the branches refer to the percentage of replicate trees that gave the depicted branch topology in a bootstrap test of 1,000 replicates. b, Distinct EET loci from select genomes are shown. Although the arrangement of genes varies, a locus with genes associated with EET is present in many genomes. Some loci contain ECF transporter ATPase subunits (homologous to those depicted in Extended Data Fig. 5a) that probably function with RibU and FmnA subunits in flavin transport. The dmkA-like gene found in Caldanaerobius fijiensis (and other genomes) lacks homology to dmkA, but is annotated as catalysing the same reaction. The pplA variant in some genomes contains a single FMNylated domain (rather than two) and this property is indicated by a shorter arrow. A few bacteria (including Lactococcus spp.) lack a recognizable locus and distribute genes associated with EET throughout the genome.

Supplementary information

Supplementary Figures

This file contains Supplementary Figure 1: Uncropped gel from Fig. 3c.

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Supplementary Tables 1-4

This file contains Supplementary Tables 1-4. Supplementary Table 1 provides proteomics evidence of the FMNylation of PplA. Supplementary Table 2 identifies surface-associated proteins in Listeria monocytogenes. Supplementary Table 3 identifies Firmicutes species with homologous EET genes. Supplementary Table 4 contains information about strains used in this study.

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Light, S.H., Su, L., Rivera-Lugo, R. et al. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Nature 562, 140–144 (2018). https://doi.org/10.1038/s41586-018-0498-z

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Keywords

  • Ferric Iron Reductase
  • Nb Fm
  • Ferric Ammonium Citrate
  • Gene Name Assignment
  • Brain Heart Infusion Medium

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