An elusive electron shuttle from a facultative anaerobe

Mevers, Emily; Su, Lin; Pishchany, Gleb; Baruch, Moshe; Cornejo, Jose A.; Hobert, Elissa M.; Dimise, Eric J.; Ajo‐Franklin, Caroline M.; Clardy, Jon

doi:10.7554/elife.48054

Cited by 63 publications

(80 citation statements)

References 19 publications

(37 reference statements)

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“…Under cathodic conditions, the current consumption by CymAMtr-expressing E. coli in the Δ menA and Δ menC backgrounds was not significantly different from the wt background ( Figure 4B, D ). These surprising observations indicate that the current consumption in Mtr-expressing E. coli does not rely on the presence of menaquinone or ACNQ, in contrast to S. oneidensis 25,32 and other reports in E. coli 35 , and that the fumarate reductase of E. coli accepts electrons either directly from MtrA or indirectly through as-yet-unknown native biomolecule inside E. coli .…”

Section: Resultsmentioning

confidence: 66%

“…CymAMtr-Δ menA) and menC 31 . menC is also essential for synthesis of the quinone-derived redox shuttle ACNQ 32 , allowing us to also test whether ACNQ is an electron carrier here. As before, these strains were acclimated in bioelectrochemical reactors under anodic conditions with similar cell densities before being switched to cathodic conditions.…”

Section: Resultsmentioning

confidence: 99%

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Precise electronic control of redox reactions inside Escherichia coli using a genetic module

Baruch

Tejedor-Sanz²,

Su³

et al. 2020

Preprint

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18Microorganisms regulate the redox state of different biomolecules to precisely control 19 biological processes. These processes can be modulated by electrochemically coupling 20 intracellular biomolecules to an external electrode, but current approaches afford only 21 limited control and specificity. Here we describe specific electrochemical control of the 22 Microorganisms accomplish important biological functions such as conserving energy, 32 regulating gene expression, and powering biosynthesis using different redox-active 33 biomolecules. To enable control of these processes in any microorganism, researchers have 34 coupled the redox state of these biomolecules to an external electrode using membrane-35 permeable, small molecule redox mediators 1-5 , redox polymers 6 , and membrane-36 intercalated nanostructures 7,8 . These approaches can allow cells to produce electrical 37 current or consume it, resulting in either oxidation or reduction of intracellular redox species, 38 respectively. Bioelectrochemical devices can then be used to drive biosynthetic reactions 39 1,4,5 , perform bioelectronic sensing 9 , actuate gene expression 3 , and modulate cellular growth 40 10,11 within the microorganism of interest. Despite these accomplishments, these strategies 41 Results 75E. coli consume current using mtr and native oxidoreductases 76 We first sought to determine if the Mtr pathway could allow cathodic electrons to 77 directly enter a heterologous host upon addition of an electron acceptor. Since E. coli has 78 two MK-linked fumarate reductases, FrdABCD and SdhABCD, we hypothesized that the Mtr 79 pathway in E. coli could deliver cathodic electrons via these native proteins to fumarate 80 ( Figure 1A). To probe the specific role of the Mtr pathway, we compared the behavior of 81 several strains: E. coli expressing only the cytochrome c maturation (ccm) genes (abbrev. 82Ccm-E.coli) 17 , E. coli expressing ccm and mtrCAB (abbrev. Mtr-E. coli) 15 , and E. coli 83 expressing ccm and cymAmtrCAB (abbrev. CymAMtr-E. coli) 17 . The ccm genes are required 84 to make cytochromes c in the C43(DE3) parental background. 85To prepare E. coli for cathodic conditions, individual strains were first grown 86 aerobically, incubated in potentiostatic-controlled bioreactors under anaerobic, anodic 87 conditions (∆V=+200 mV Ag/AgCl ) for at least one day. Under these conditions, the CymAMtr-88 E. coli strain produced a significant steady-state current, while Ccm-E. coli and Mtr-E. coli 89 produced much lower currents (Figure 2A), reinforcing that CymA is important for current 90 production [16][17][18] . As anaerobic conditions were maintained, the electrode bias was then 91 switched to cathodic conditions (∆V= -560 V Ag/AgCl ), fumarate was added, and current 92 consumption was measured. In the absence of E. coli, neither current consumption nor 93 fumarate reduction was observed (Figure S1A). Likewise, the Ccm-E. coli strain did not 94 consume significant levels of current (Figure 2B). In contrast, both the Mtr-E. coli and t...

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Section: Resultsmentioning

confidence: 66%

Section: Resultsmentioning

confidence: 99%

Precise electronic control of redox reactions inside Escherichia coli using a genetic module

Baruch

Tejedor-Sanz²,

Su³

et al. 2020

Preprint

Self Cite

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“…For example, flavins can stimulate EET by Shewanella oneidensis and Listeria monocytogenes (101,102). Similarly, diverse quinones can stimulate EET by Klebsiella pneumonia, Lactococcus lactis, Shewanella oneidensis and Sphingomonas xenophaga (103)(104)(105)(106). Bioinformatic analysis indicates that hundreds of species from the phyla Actinobacteria and Proteobacteria contain phenazine biosynthetic clusters (65,107).…”

Section: A General Hypothesis For Ram-mediated Survivalmentioning

confidence: 99%

The Potential for Redox-Active Metabolites To Enhance or Unlock Anaerobic Survival Metabolisms in Aerobes

Ciemniecki

Newman

2020

J Bacteriol

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Classifying microorganisms as “obligate” aerobes has colloquially implied death without air, leading to the erroneous assumption that, without oxygen, they are unable to survive. However, over the past few decades, more than a few obligate aerobes have been found to possess anaerobic energy conservation strategies that sustain metabolic activity in the absence of growth or at very low growth rates. Similarly, studies emphasizing the aerobic prowess of certain facultative aerobes have sometimes led to underrecognition of their anaerobic capabilities. Yet an inescapable consequence of the affinity both obligate and facultative aerobes have for oxygen is that the metabolism of these organisms may drive this substrate to scarcity, making anoxic survival an essential skill. To illustrate this, we highlight the importance of anaerobic survival strategies for Pseudomonas aeruginosa and Streptomyces coelicolor, representative facultative and obligate aerobes, respectively. Included among these strategies, we describe a role for redox-active secondary metabolites (RAMs), such as phenazines made by P. aeruginosa, in enhancing substrate-level phosphorylation. Importantly, RAMs are made by diverse bacteria, often during stationary phase in the absence of oxygen, and can sustain anoxic survival. We present a hypothesis for how RAMs may enhance or even unlock energy conservation pathways that facilitate the anaerobic survival of both RAM producers and nonproducers.

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“…The role of this unidentified molecule has been the subject of debate: is it shuttling electrons to acceptors outside of the bacteria, or is it an intermediate in menaquinone synthesis that can fix the defect in mutant S. oneidensis ? Now, in eLife, and nearly twenty years after its initial description, Jon Clardy and colleagues – including Emily Mevers and Lin Su as joint first authors – report that they have identified this molecule as ACNQ (2-amino-3-carboxyl-1,4-napthoquinone), a soluble analogue of menaquinone that can work as an electron shuttle (Mevers et al, 2019).…”

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confidence: 99%

“…However, genetic analysis of S. oneidensis and E. coli did not yield any candidate enzymes that could produce ACNQ. This led to the intriguing hypothesis that ACNQ is synthetized from DHNA without the help of enzymes (Mevers et al, 2019). And indeed, Mevers et al showed that, in a sterile medium, DHNA and an ammonia source could react to form ACNQ, demonstrating that the molecule could be created through an abiotic mechanism (Figure 1B).…”

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confidence: 99%