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Cited by 80Per- and polyfluoroalkyl substances researchFluorine in Organic ChemistryFluoride Effects and Removal

The DOI matches its Crossref record; 131 of the 131 references it cites were found in a registry or an index; none of the 178 sources its claims cite is checked for support yet.

The link between ancient microbial fluoride resistance mechanisms and bioengineering organofluorine degradation or synthesis

Open access
Stockbridge, Randy B., Wackett, Lawrence P.·2024·Nature Communications
DOI 10.1038/s41467-024-49018-1PMC PMC11139923
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Abstract

Fluorinated organic chemicals, such as per- and polyfluorinated alkyl substances (PFAS) and fluorinated pesticides, are both broadly useful and unusually long-lived. To combat problems related to the accumulation of these compounds, microbial PFAS and organofluorine degradation and biosynthesis of less-fluorinated replacement chemicals are under intense study. Both efforts are undermined by the substantial toxicity of fluoride, an anion that powerfully inhibits metabolism. Microorganisms have contended with environmental mineral fluoride over evolutionary time, evolving a suite of detoxification mechanisms. In this perspective, we synthesize emerging ideas on microbial defluorination/fluorination and fluoride resistance mechanisms and identify best approaches for bioengineering new approaches for degrading and making organofluorine compounds.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

This Perspective argues that fluoride toxicity, not only C–F bond strength, is a central bottleneck for microbial organofluorine degradation and biosynthesis. It synthesizes ancient microbial fluoride-resistance mechanisms and proposes bioengineering, adaptive evolution, and growth-condition strategies to improve PFAS bioremediation and fluorinated-compound synthesis.

Key findings

  • Fluoride strongly inhibits central metabolism: enzyme \(K_i\) values are typically ~100 μM, enolase is inhibited at ~80 μM, wild-type bacteria respond at intracellular fluoride around 60 μM and extracellular concentrations as low as 200 μM, and engineered *Pseudomonas putida* growing on fluorinated substrates accumulated fluoride in medium above 50 mM.
  • Fluoride exporters are ancient and widespread: >85% of surveyed GEBA representative prokaryotic genomes possess a fluoride exporter, CLCF and Fluc exporters are usually mutually exclusive with only ~3% of strains possessing both, Fluc channels efflux at ~10^6 ions/s with >10,000-fold fluoride selectivity, and CLCFs are >80-fold selective for fluoride over chloride.
  • Fluoride stress also constrains biosynthesis: the well-studied *Streptomyces cattleya* fluorinase has \(k_{cat}\) up to 0.4 min⁻¹ and a fluoride \(K_m\) of 2 mM, requiring cells to tolerate intracellular fluoride levels far above those that trigger stress responses.
  • The paper recommends using naturally fluoride-resistant hosts, adaptive evolution/acclimation, engineering fluoride exporters or fluoride-sensitive enzymes, optimizing pH/phosphate/divalent-cation/antioxidant conditions, and integrating fluorobiosynthesis with fluoride tolerance.

Methods

  • Design: a Perspective/review that synthesizes emerging ideas on microbial defluorination/fluorination and fluoride resistance; no new primary experimental data are reported.
  • Data/sample: cited literature plus a comparative genomic survey of the Joint Genome Institute GEBA representative prokaryotic genomes, and a compiled table of fluoride resistance phenotypes and transport rates.
  • Analysis: narrative synthesis of microbial physiology, enzymology, and bioengineering proposals, with comparative genomics used to describe fluoride exporter distribution.

Limitations

  • Stated: the authors note that they are “not aware of any systematic investigation of fluoride acclimation in bacteria,” that molecular mechanisms of fluoride sequestration are “not as well understood,” and that in some reported PFAS-degradation studies “no enzymes were directly identified.”
  • Evident: as a Perspective, it does not perform a systematic review or new experiments, and several recommendations are explicitly theoretical or proposed rather than demonstrated.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1038/s41467-024-49018-1

Cites

131 of 131 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

0 of 178 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The authors have measured enzymatic C-F bond cleavage in one instance to be as fast as 10 bonds cleaved per second per enzyme.

    “We have measured enzymatic C–F bond cleavage in one instance to be as fast as 10 bonds cleaved per second per enzyme (and there are thousands of enzymes per cell).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: There are thousands of enzymes per cell.
  • Premisecitation

    The ionic form of fluoride becomes trapped in the cell, accumulating to levels dictated by the pH gradient across the membrane.

    “The ionic form becomes trapped in the cell, accumulating to levels dictated by the pH gradient across the membrane71.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [71] Ji, C., Stockbridge, R. B. & Miller, C. Bacterial fluoride resistance, Fluc channels, and the weak acid accumulation effect. J. Gen. Physiol. 144, 257–261 (2014). This study quantitatively showed the interplay between pH, intracellular fluoride, and fitness in bacterial populations. source
  • Premisecitation

    Fluorinase catalyzes the reaction of fluoride anion and S-adenosyl-L-methionine (SAM) to make 5′-fluoro-5′deoxyadenosine (5′-FDA) and L-methionine.

    “Nature offers the enzyme fluorinase, which catalyzes the reaction of fluoride anion and S-adenosyl-L-methionine (SAM) to make 5′-fluoro-5′deoxyadenosine (5′-FDA) and L-methionine53.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [53] Dong, C. et al. Crystal structure and mechanism of a bacterial fluorinating enzyme. Nature 427, 561–565 (2004). source
  • Premisecitation

    WT bacteria mount a gene expression response at intracellular fluoride concentrations around 60 μM.

    “Congruent with this, WT bacteria mount a gene expression response at intracellular fluoride concentrations around 60 μM67, and extracellular concentrations as low as 200 μM68.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source
  • Interpretationreasoning

    The mM Km values of fluorinase for fluoride require that cells tolerate intracellular fluoride levels 100-fold greater than those that begin to elicit fluoride stress responses.

    “The mM Km values of fluorinase for fluoride require that cells tolerate intracellular fluoride levels 100-fold greater than those that begin to elicit fluoride stress responses.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim. 27
  • It may state two separate claims as one. 38

  • Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds.

    Interpretationreasoning

    Fluoroacetate production is thought to be an ancient function given the geographic and taxonomic distribution of the fluoroacetate producers.

    “Fluoroacetate production is thought to be an ancient function given the geographic and taxonomic distribution of the fluoroacetate producers.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    Fluorinated organic chemicals such as PFAS and fluorinated pesticides are broadly useful and unusually long-lived.

    “Fluorinated organic chemicals, such as per- and polyfluorinated alkyl substances (PFAS) and fluorinated pesticides, are both broadly useful and unusually long-lived.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [3] Evich, M. G. et al. Per- and polyfluoroalkyl substances in the environment. Science 375, 512 (2022). This comprehensive current review conveys the scale of PFAS environmental contamination and exposure, and the burden of remediation. source

  • It may state two separate claims as one.

    Premisereasoning

    HF is membrane permeant but dissociates to H+ and F− at the physiological cytoplasmic pH.

    “HF is membrane permeant but dissociates to H+ and F− at the physiological cytoplasmic pH.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim. It may be too vague to check against evidence. The paper’s conclusions may not depend on it. The paper may give no reason why it holds.

    Interpretationnone given

    Biologically-generated replacement chemicals could be designed to have less toxicity and greater biodegradability.

    “Likewise, biologically-generated replacement chemicals could be designed to have less toxicity and greater biodegradability.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Biologically-generated replacement chemicals could be designed to have less toxicity and greater biodegradability.

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    Globally, almost the entire human population has detectable blood serum levels of PFAS.

    “Globally, almost the entire human population has detectable blood serum levels of PFAS8, in major part due to environmental exposure from water or food sources12.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [8] Fenton, S. E. et al. Per- and polyfluoroalkyl substance toxicity and human health review: current state of knowledge and strategies for informing future research. Environ. Toxicol. Chem. 40, 606–630 (2021). source

  • Probably not a substantial claim. The paper may give no reason why it holds.

    Premisenone given

    Fluoride cannot passively diffuse across the membrane.

    “Because fluoride cannot passively diffuse across the membrane, if this reaction occurs in the cytoplasm, fluoride will accumulate intracellularly.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Fluoride cannot passively diffuse across the membrane.

  • It may state two separate claims as one.

    Interpretationcitation

    Fluoroacetate dehalogenases were selected for fluoroacetate detoxification or assimilation of fluoroacetate as a carbon source.

    “These fluoroacetate dehalogenases prefer fluorine over other halogen substituents, suggesting that they were selected for fluoroacetate detoxification or assimilation of fluoroacetate as a carbon source30,33.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [30] Goldman, P. The enzymatic cleavage of the carbon-fluorine bond in fluoroacetate. J. Biol. Chem. 240, 3434–3438 (1965). source
    • cites [33] Heffernan, B., Murphy, C. D. & Casey, E. Comparison of planktonic and biofilm cultures of Pseudomonas fluorescens DSM 8341 cells grown on fluoroacetate. Appl. Environ. Microbiol 75, 2899–2907 (2009). source

  • It may state two separate claims as one.

    Premisecitation

    Defluorination of perfluorinated acids has been reported in consortia and by a single bacterium.

    “Biological systems that degrade perfluorinated compounds have also been reported recently44,45, including reports of the defluorination of perfluorinated acids in consortia46–48 and by a single bacterium49.”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [46] Yu, Y. C. et al. Microbial cleavage of C-F bonds in two C6 per- and polyfluorinated compounds via reductive defluorination. Environ. Sci. Technol. 54, 14393–14402 (2020). This study establishes the reductive defluorination of perfluorinated compounds by microbial consortia. source
    • cites [47] Jin, B. S. et al. Aerobic biotransformation and defluorination of fluoroalkylether substances (ether PFAS): substrate specificity, pathways, and applications. Environ. Sci. Technol. Lett. 10, 755–761 (2023). source
    • cites [48] Wang, N., Buck, R. C., Szostek, B., Sulecki, L. M. & Wolstenholme, B. W. 5:3 Polyfluorinated acid aerobic biotransformation in activated sludge via novel “one-carbon removal pathways”. Chemosphere 87, 527–534 (2012). source
    • cites [49] Huang, S. & Jaffe, P. R. Defluorination of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) by Acidimicrobium sp. strain A6. Environ. Sci. Technol. 53, 11410–11419 (2019). source

  • It may state two separate claims as one.

    Premisecitation

    Biosynthesis of fluoroacetate in E. coli requires not only the biosynthetic genes from S. cattleya, but also chromosomal knockouts of the crcB gene, which encodes a fluoride channel.

    “For example, biosynthesis of fluoroacetate in E. coli requires not only the biosynthetic genes from S. cattleya, but also chromosomal knockouts of the crcB gene, which encodes a fluoride channel64.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [64] Markakis, K. et al. An engineered E. coli strain for direct in vivo fluorination. Chembiochem 21, 1856–1860 (2020). source

  • It may state two separate claims as one.

    Interpretationreasoning

    Although perfluorinated organic compounds are an anthropogenic stressor, fluoride resistance mechanisms are ancient and diverse.

    “Although perfluorinated organic compounds are an anthropogenic stressor, fluoride resistance mechanisms are ancient and diverse (Fig. 2).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    Over the last 22 years, more than 50% of newly registered pesticides are organofluorine compounds.

    “For example, over the last 22 years, more than 50% of newly registered pesticides are organofluorine compounds6.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [6] Ogawa, Y., Tokunaga, E., Kobayashi, O., Hirai, K. & Shibata, N. Current contributions of organofluorine compounds to the agrochemical industry. Iscience 23, 101467 (2020). source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    Fluorine is more common in the earth's crust than phosphorus, nitrogen, and sulfur.

    “Fluorine is more common in the earth’s crust than phosphorus, nitrogen, and sulfur and yet a survey of the elemental composition of several dozen prokaryotes did not identify fluorine amongst the 33 elements found, making it less prevalent than non-biological metals like cadmium, tin, and silver23.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [23] Novoselov, A. A. et al. From cytoplasm to environment: the inorganic ingredients for the origin of life. Astrobiology 13, 294–302 (2013). source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Interpretationreasoning

    A plausible degradative pathway for perfluorocarboxylic acids would use consecutive paired reactions of α,α-defluorination and decarboxylation, releasing fluoride ions at each step and culminating in trifluoroacetic acid.

    “Since α-keto acid decarboxylases are known, a plausible degradative pathway for perfluorocarboxylic acids would use consecutive paired reactions of α,α-defluorination and decarboxylation, releasing fluoride ions at each step and culminating in trifluoroacetic acid, an end product that is highly recalcitrant to further degradation.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    Fluorine in the earth's crust is largely found as fluoride bound in mineral form, for example fluorite, fluorapatite, topaz, cryolite, sellaite, and villiaumite.

    “Fluorine in the earth’s crust is largely found as fluoride bound in mineral form, for example: fluorite, fluorapatite, topaz, cryolite, sellaite, and villiaumite74.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [74] Fuge, R. Fluorine in the environment, a review of its sources and geochemistry. Appl. Geochem. 100, 393–406 (2019). source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    Fluoroacetate becomes highly toxic to central metabolism after metabolic conversion to fluorocitrate.

    “Plants of several varieties in Australia, Africa, and South America produce fluoroacetate to deter feeding by animals, since the compound becomes highly toxic to central metabolism after metabolic conversion to fluorocitrate24,25.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [24] Walsh, C. Fluorinated substrate analogs: routes of metabolism and selective toxicity. Adv. Enzymol. Relat. Areas Mol. Biol. 55, 197–289 (1983).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

    • cites [25] Marais, J. S. C. The isolation of the toxic principle “potassium cymonate” from “Gifblaar” Dichapetalum cymosum. Onderstepoort J. Vet. Sci. Anim. Ind. 18, 203–206 (1943).

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    PFAS blood serum levels are in major part due to environmental exposure from water or food sources.

    “Globally, almost the entire human population has detectable blood serum levels of PFAS8, in major part due to environmental exposure from water or food sources12.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [12] Sunderland, E. M. et al. A review of the pathways of human exposure to poly- and perfluoroalkyl substances (PFASs) and present understanding of health effects. J. Expo. Sci. Environ. Epidemiol. 29, 131–147 (2019). source

  • Probably not a substantial claim. The paper may give no reason why it holds.

    Premisenone given

    Biological syntheses use NaF.

    “In particular, organofluorine degradation yields fluoride ions, and biological syntheses use NaF.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim. It may be too vague to check against evidence.

    Interpretationreasoning

    Applying fundamental physiological considerations to bioengineer solutions to PFAS and organofluorine persistence can help circumvent some common roadblocks.

    “We argue that applying fundamental physiological considerations to bioengineer solutions to PFAS and organofluorine persistence can help circumvent some of the common roadblocks that have emerged in these fields of study.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim. The paper may give no reason why it holds.

    Interpretationnone given

    Bioremediation would be cheaper and more effective than physico-chemical remediation in some circumstances if suitable biological systems can be identified or engineered.

    “Bioremediation would be cheaper and more effective than physico-chemical remediation in some circumstances if suitable biological systems can be identified or engineered.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Bioremediation would be cheaper and more effective than physico-chemical remediation in some circumstances if suitable biological systems can be identified or engineered.

  • It may state two separate claims as one.

    Premisecitation

    Enolase is often observed in operons controlled by fluoride riboswitches, and in fluoride-resistant E. cloacae FRM, enolase transcripts are upregulated 176-fold in response to fluoride.

    “Enolase is often observed in operons controlled by fluoride riboswitches67, and in fluoride-resistant E. cloacae FRM, enolase transcripts are upregulated 176-fold in response to fluoride95.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source
    • cites [95] Liu, X. et al. Identification of an operon involved in fluoride resistance in Enterobacter cloacae FRM. Sci. Rep. 7, 6786 (2017). source

  • It may state two separate claims as one.

    Premisecitation

    No systematic investigation of fluoride acclimation in bacteria has been conducted, but fluoride acclimation over multiple generations yielded S. cerevisiae strains with ~700-fold better fluoride resistance, independent of fluoride exporter expression.

    “We are not aware of any systematic investigation of fluoride acclimation in bacteria, but the example of S. cerevisiae is encouraging, as fluoride acclimation over multiple generations yielded strains with ~700-fold better fluoride resistance, independent of fluoride exporter expression88.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [88] Strobel, S. A., Johnston, N. R. & Cline, G. Cells adapt to resist fluoride through metabolic deactivation and intracellular acidification. Chem. Res. Toxicol. 35, 2085–2096 (2022). By acclimating yeast to high fluoride over several generations, this study uncovered several novel fluoride stress mitigation mechanisms in microbes. source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    Formate hydrogen lyase is another of the most common fluoride riboswitch-associated enzymes.

    “Formate hydrogen lyase, which oxidizes formic acid to produce ATP during anaerobic sugar fermentation, is another of the most common fluoride riboswitch-associated enzymes67.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source

  • It may state two separate claims as one.

    Premisecitation

    Fluoride stress causes changes to cell morphology, including cell shortening or lack of separation following septation, and increased extracellular carbohydrate content.

    “Similarly, changes to cell morphology, including cell shortening or lack of separation following septation, and increased extracellular carbohydrate content, are also caused by fluoride stress63,107,108.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [63] Dodge, A. G., Thoma, C. J., O’Connor, M. R. & Wackett, L. P. Recombinant Pseudomonas growing on non-natural fluorinated substrates shows stress but overall tolerance to cytoplasmically released fluoride anion. mBio 15, e0278523 (2023). This article directly demonstrates fluoride toxicity due to intracellular enzymatic defluorination, with multiple signs of cellular stress. source
    • cites [107] Evans, K., Stone, V., Chen, L., Ge, X. C. & Xu, P. Systematic study of genes influencing cellular chain length in Streptococcus sanguinis. Microbiology 160, 307–315 (2014). source
    • cites [108] Mukherjee, S., Sahu, P. & Halder, G. Microbial remediation of fluoride-contaminated water via a novel bacterium Providencia vermicola (KX926492). J. Environ. Manag. 204, 413–423 (2017). source

  • Probably not a substantial claim. The paper may give no reason why it holds. It may state two separate claims as one.

    Interpretationreasoning

    Fluoride tolerance is required for the synthesis of organofluorine chemicals, since fluoride ions must be supplied to bacteria for fluorination reactions.

    “Likewise, fluoride tolerance is required for the synthesis of organofluorine chemicals, since fluoride ions must be supplied to bacteria for fluorination reactions.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.

    Premisecitation

    Fluc proteins can be encoded by single genes forming antiparallel homodimers, or by paired genes forming heterodimers of obligate inward- and outward-facing subunits.

    “Fluc proteins can be encoded by single genes, in which case a single protomer is inserted into the membrane in both inward and outward-facing conformations, assembling as an antiparallel homodimer, or they can be encoded by paired genes that express to form heterodimers of obligate inward- and outward-facing subunits84.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [84] Macdonald, C. B. & Stockbridge, R. B. A topologically diverse family of fluoride channels. Curr. Opin. Struct. Biol. 45, 142–149 (2017). source

  • It may state two separate claims as one.

    Premisecitation

    The gene encoding pyrophosphatase is among the genes most frequently associated with fluoride riboswitches, and in various organisms, expression of pyrophosphatase, polyphosphatase, and phosphate importers has been functionally linked to fluoride resistance.

    “The gene encoding pyrophosphatase is among the genes most frequently associated with fluoride riboswitches67, and in various organisms, including Enterobacter cloacae FRM95, Acidithiophilus ferredoxins96, and S. cerevisiae97, the expression of pyrophosphatase, polyphosphatase, and phosphate importers has been functionally linked to fluoride resistance.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source
    • cites [95] Liu, X. et al. Identification of an operon involved in fluoride resistance in Enterobacter cloacae FRM. Sci. Rep. 7, 6786 (2017). source
    • cites [96] Ma, L. Y. et al. Insights into the fluoride-resistant regulation mechanism of Acidithiobacillus ferrooxidans ATCC 23270 based on whole genome microarrays. J. Ind. Microbiol. Biotechnol. 43, 1441–1453 (2016). source

  • Probably not a substantial claim. The paper may give no reason why it holds.

    Interpretationreasoning

    Although this review focuses on bacteria, fluoride stress responses are ancient and conserved, at least in part, among microorganisms.

    “Although this review focuses on bacteria, fluoride stress responses are ancient and conserved, at least in part, among microorganisms.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    After fluoride exporters, the next-most common class of riboswitch-associated genes is Na+/H+ antiporters, which contribute to pH homeostasis in bacteria.

    “Indeed, after fluoride exporters, the next-most common class of riboswitch-associated genes is Na+/H+ antiporters67, which contribute to pH homeostasis in bacteria94.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source
    • cites [94] Zilberstein, D., Agmon, V., Schuldiner, S. & Padan, E. The sodium proton antiporter is part of the pH homeostasis mechanism in Escherichia coli. J. Biol. Chem. 257, 3687–3691 (1982). source

  • It may state two separate claims as one.

    Interpretationreasoning

    Maintaining pH homeostasis is important for fluoride resistance in microorganisms, and acid stress-response pathways are commonly upregulated in response to fluoride.

    “As a result, maintaining pH homeostasis is important for fluoride resistance in microorganisms, and acid stress-response pathways are commonly upregulated in response to fluoride88,93.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [88] Strobel, S. A., Johnston, N. R. & Cline, G. Cells adapt to resist fluoride through metabolic deactivation and intracellular acidification. Chem. Res. Toxicol. 35, 2085–2096 (2022). By acclimating yeast to high fluoride over several generations, this study uncovered several novel fluoride stress mitigation mechanisms in microbes. source
    • cites [93] Johnston, N. R., Nallur, S., Gordon, P. B., Smith, K. D. & Strobel, S. A. Genome-wide identification of genes involved in general acid stress and fluoride toxicity in Saccharomyces cerevisiae. Front. Microbiol. 11, 1410 (2020). source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.

    Premisecitation

    Typically, genes for heterodimeric Flucs are adjacent in genomes, and both genes are required for fluoride efflux activity.

    “Typically, the genes for the heterodimeric Flucs are adjacent to each other in genomes, and both genes are required for fluoride efflux activity84.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [84] Macdonald, C. B. & Stockbridge, R. B. A topologically diverse family of fluoride channels. Curr. Opin. Struct. Biol. 45, 142–149 (2017). source

  • It may state two separate claims as one.

    Interpretationreasoning

    Fluoride export is dependent on the proton-motive force, either as an explicit chemical driving force for CLCFs or as a component of the electrical gradient for Flucs.

    “In addition, fluoride export is dependent on the proton-motive force – either as an explicit chemical driving force for the CLCFs, or as a component of the electrical gradient, as for the Flucs.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    Fluoride-acclimated S. cerevisiae exhibited increased clumping and mutations to genes associated with flocculation, pseudohyphal growth, cell surface properties, and adhesion.

    “Fluoride-acclimated S. cerevisiae exhibited increased clumping and mutations to genes associated with flocculation, pseudohyphal growth, cell surface properties, and adhesion88.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [88] Strobel, S. A., Johnston, N. R. & Cline, G. Cells adapt to resist fluoride through metabolic deactivation and intracellular acidification. Chem. Res. Toxicol. 35, 2085–2096 (2022). By acclimating yeast to high fluoride over several generations, this study uncovered several novel fluoride stress mitigation mechanisms in microbes. source

  • It may state two separate claims as one.

    Interpretationreasoning

    Sequestration can be used as a fluoride mitigation strategy by biology and could be stimulated by divalent metal and phosphate uptake.

    “Thus, sequestration can be used as a fluoride mitigation strategy by biology, and, in principle, could be stimulated by the divalent metal and phosphate uptake described above.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    FEX proteins are structurally related to Flucs but possess a more complex two-domain fold.

    “FEX proteins are related structurally to the Flucs but possess a more complex two-domain fold83,87.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [83] Stockbridge, R. B. et al. Crystal structures of a double-barrelled fluoride ion channel. Nature 525, 548–551 (2015). source
    • cites [87] Smith, K. D. et al. Yeast Fex1p is a constitutively expressed fluoride channel with functional asymmetry of its two homologous domains. J. Biol. Chem. 290, 19874–19887 (2015). source

  • It may state two separate claims as one.

    Premisecitation

    In yeast, fluoride resistance is imparted by the export of compounds like nitrates that contribute to oxidative stress, and the import of antioxidant metabolites like sulfite.

    “In yeast, fluoride resistance is imparted by the export of compounds like nitrates that contribute to oxidative stress, and the import of antioxidant metabolites like sulfite97.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [97] Johnston, N. R. & Strobel, S. A. Nitrate and phosphate transporters rescue fluoride toxicity in yeast. Chem. Res. Toxicol. 32, 2305–2319 (2019). source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds. It may state two separate claims as one.

    Interpretationnone given

    One natural mechanism of fluoride resistance is metabolic deactivation, which may be at odds with the end goal of improving fluoride resistance in order to metabolize fluorinated substrates.

    “However, it should be noted that one natural mechanism of fluoride resistance is metabolic deactivation, which may be at odds with the end goal of improving fluoride resistance in order to metabolize fluorinated substrates.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    Among oral streptococci, fluoride inhibits lectins that shape biofilm architecture and increases turnover of cell wall peptidoglycans, contributing to cellular lysis.

    “Among the oral streptococci, fluoride has been shown to inhibit lectins that shape biofilm architecture105, and increase turnover of cell wall peptidoglycans, contributing to cellular lysis106.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [105] Cox, S. D., Lassiter, M. O., Taylor, K. G. & Doyle, R. J. Fluoride inhibits the glucan-binding lectin of Streptococcus sobrinus. FEMS Microbiol. Lett. 123, 331–334 (1994). source
    • cites [106] Lesher, R. J., Bender, G. R. & Marquis, R. E. Bacteriolytic action of fluoride ions. Antimicrob. Agents Chemother. 12, 339–345 (1977). source

  • It may state two separate claims as one.

    Premisecitation

    Fluoride-adapted S. cerevisiae exhibit metabolic shifts to anaerobic fermentation pathways and are depleted in TCA cycle intermediates.

    “Fluoride-adapted S. cerevisiae also exhibit metabolic shifts to anaerobic fermentation pathways, and like P. putida, are depleted in TCA cycle intermediates88.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [88] Strobel, S. A., Johnston, N. R. & Cline, G. Cells adapt to resist fluoride through metabolic deactivation and intracellular acidification. Chem. Res. Toxicol. 35, 2085–2096 (2022). By acclimating yeast to high fluoride over several generations, this study uncovered several novel fluoride stress mitigation mechanisms in microbes. source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.

    Premisecitation

    Flucs are the most selective ion channel yet described, and no role besides fluoride export has been ascribed to any protein in this family.

    “The Flucs are the most selective ion channel yet described, and no role besides fluoride export has been ascribed to any protein in this family65.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [65] McIlwain, B. C., Ruprecht, M. T. & Stockbridge, R. B. Membrane exporters of fluoride ion. Annu. Rev. Biochem. 90, 559–579 (2021). This work reviews biochemical mechanisms of fluoride toxicity, along with the structures and mechanisms of microbial fluoride exporters that maintain cytoplasmic fluoride at sub-inhibitory concentrations. source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premiseown data

    The CLCF and Fluc proteins are usually mutually exclusive in bacterial genomes.

    “The CLCF and Fluc proteins are usually mutually exclusive in bacterial genomes; only ~3% of strains surveyed possess both.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    E. coli appears to shut down metabolism entirely under fluoride, only resuming growth once the fluoride insult is removed.

    “Other bacteria, like E. coli, appear to shut down metabolism entirely, only resuming growth once the fluoride insult is removed71.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [71] Ji, C., Stockbridge, R. B. & Miller, C. Bacterial fluoride resistance, Fluc channels, and the weak acid accumulation effect. J. Gen. Physiol. 144, 257–261 (2014). This study quantitatively showed the interplay between pH, intracellular fluoride, and fitness in bacterial populations. source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it. The paper may give no reason why it holds. It may state two separate claims as one.

    Interpretationnone given

    Fluoride chelation impacts ion homeostasis, especially for divalent cations, and these perturbations can contribute to oxidative stress.

    “Fluoride chelation impacts ion homeostasis, especially for divalent cations, and these perturbations can contribute to oxidative stress.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    The most common proteins found in operons with fluoride riboswitches are fluoride exporters, although only ~15% of Flucs and ~30% of CLCFs are regulated by riboswitches.

    “The most common proteins found in operons with these riboswitches are the fluoride exporters67, although only ~15% of Flucs and ~30% of CLCFs are regulated by riboswitches.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source

  • It may state two separate claims as one.

    Interpretationreasoning

    Although fluoride exporters contribute most to fluoride resistance, different organisms exhibit substantial variability in tolerated fluoride concentrations, suggesting additional physiological determinants of fluoride resistance.

    “Although the fluoride exporters contribute most to fluoride resistance, different organisms still exhibit substantial variability in the fluoride concentrations that they tolerate (Table 1), suggesting that there are additional physiological determinants of fluoride resistance.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Table 1

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • It may state two separate claims as one.

    Premisecitation

    A fluoride-resistant strain of S. mutans exhibits constitutive expression of CLCF genes, and a single nucleotide polymorphism in the intergenic region 5′ to the operon was linked to this mechanism.

    “A fluoride-resistant strain of S. mutans exhibits a constitutive expression of the CLCF genes, and a single nucleotide polymorphism in the intergenic region 5′ to the operon was linked to this mechanism91.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [91] Liao, Y. et al. Identification and functional analysis of genome mutations in a fluoride-resistant Streptococcus mutans strain. PLoS ONE 10, e0122630 (2015). source

  • It may state two separate claims as one.

    Premisecitation

    The best-studied regulatory element is the fluoride riboswitch, which binds fluoride as a fluoride-magnesium complex and upregulates transcription of downstream genes.

    “The best-studied regulatory element is the fluoride riboswitch, which binds fluoride as a fluoride-magnesium complex and upregulates the transcription of downstream genes67,89.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source
    • cites [89] Ren, A., Rajashankar, K. R. & Patel, D. J. Fluoride ion encapsulation by Mg2+ ions and phosphates in a fluoride riboswitch. Nature 486, 85–89 (2012). source

  • It may state two separate claims as one.

    Premisecitation

    Some plants accumulate fluoride as insoluble calcium or magnesium complexes in the vacuole, and fluoride-acclimated yeast exhibited far lower soluble calcium compared to total calcium, suggesting calcium's presence in an insoluble form.

    “For example, some plants accumulate fluoride as insoluble calcium or magnesium complexes in the vacuole121, and fluoride-acclimated yeast exhibited far lower soluble calcium compared to total calcium, suggesting calcium’s presence in an insoluble form88.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [121] Baunthiyal, M. & Ranghar, S. Accumulation of fluoride by plants: potential for phytoremediation. Clean.-Soil Air Water 43, 127–132 (2015). source
    • cites [88] Strobel, S. A., Johnston, N. R. & Cline, G. Cells adapt to resist fluoride through metabolic deactivation and intracellular acidification. Chem. Res. Toxicol. 35, 2085–2096 (2022). By acclimating yeast to high fluoride over several generations, this study uncovered several novel fluoride stress mitigation mechanisms in microbes. source

  • It may state two separate claims as one.

    Premisecitation

    Membrane permeation of the weak acid HF is the major route to fluoride accumulation in the cytosol, and fluoride exposure is correlated with cytoplasmic acidification.

    “Since membrane permeation of the weak acid HF is the major route to fluoride accumulation in the cytosol92, fluoride exposure is correlated with cytoplasmic acidification21.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [92] Marquis, R. E., Clock, S. A. & Mota-Meira, M. Fluoride and organic weak acids as modulators of microbial physiology. FEMS Microbiol. Rev. 26, 493–510 (2003). source
    • cites [21] Calero, P., Gurdo, N. & Nikel, P. I. Role of the CrcB transporter of Pseudomonas putida in the multi-level stress response elicited by mineral fluoride. Environ. Microbiol. 24, 5082–5104 (2022). source

  • It may state two separate claims as one.

    Premisecitation

    Flucs have a rapid rate of F− efflux (10^6 ions/s) and extremely high selectivity for fluoride over other anions, exceeding 10,000-fold.

    “The Flucs are notable for their rapid rate of F− efflux (106 ions/s) and extremely high selectivity for fluoride over other anions, which exceeds 10,000-fold81,82.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [81] Stockbridge, R. B., Robertson, J. L., Kolmakova-Partensky, L. & Miller, C. A family of fluoride-specific ion channels with dual-topology architecture. eLife 2, e01084 (2013). source
    • cites [82] McIlwain, B. C., Gundepudi, R., Koff, B. B. & Stockbridge, R. B. The fluoride permeation pathway and anion recognition in Fluc family fluoride channels. eLife 10, e69482 (2021). source

  • It may state two separate claims as one.

    Premisecitation

    The gene encoding chorismate mutase is one of the most common genes in fluoride exporter gene neighborhoods, and its expression is upregulated in fluoride-resistant S. mutans together with the fluoride exporters in the same operon.

    “The gene encoding chorismate mutase, a key enzyme in the biosynthesis of aromatic amino acids, is one of the most common genes in fluoride exporter gene neighborhoods67, and its expression is upregulated in fluoride-resistant S. mutans together with the fluoride exporters in the same operon91.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [67] Baker, J. L. et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335, 233–235 (2012). This is the first study to establish a molecular basis for the fluoride stress response. source
    • cites [91] Liao, Y. et al. Identification and functional analysis of genome mutations in a fluoride-resistant Streptococcus mutans strain. PLoS ONE 10, e0122630 (2015). source

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    A SAM regenerating system has been developed for the purpose of supporting in vitro cobalamin biosynthesis.

    “A SAM regenerating system has been developed for the purpose of supporting in vitro cobalamin biosynthesis and this could be useful in fluorinase biochemistry, too131.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [131] Xiao, K. X. et al. Optimization of hydrogenobyrinic acid synthesis in a cell-free multienzyme reaction by novel S-adenosyl-methionine regeneration. ACS Synth. Biol. 12, 1339–1348 (2023). source

  • It may state two separate claims as one.

    Premiseown data

    Fluc channels are more widely distributed among diverse bacteria than CLCF transporters, and Flucs are found more commonly in strains that resist high fluoride or that use fluoride for synthesis.

    “Fluc channels are more widely distributed among diverse bacteria than CLCF transporters (Fig. 3), and Flucs are found more commonly in strains that resist high fluoride or that use fluoride for synthesis.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Fig. 3

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim. The paper’s conclusions may not depend on it.

    Premisecitation

    A variety of fluoride-binding materials have been developed for treating potable waters that naturally contain high levels of fluoride.

    “A variety of fluoride-binding materials have been developed for treating potable waters that naturally contain high levels of fluoride128.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [128] Tolkou, A. K., Manousi, N., Zachariadis, G. A., Katsoyiannis, I. A. & Deliyanni, E. A. Recently developed adsorbing materials for fluoride removal from water and fluoride analytical determination techniques: a review. Sustainability 13, 7061 (2021). source

  • It may state two separate claims as one.

    Interpretationreasoning

    The F−/H+ antiport mechanism couples fluoride export to the proton gradient, sustaining a lower intracellular fluoride concentration at equilibrium, whereas fluoride channels have the advantage of more rapid fluoride removal that does not depend on a proton gradient.

    “The F−/H+ antiport mechanism couples fluoride export to the proton gradient, sustaining a lower intracellular fluoride concentration at equilibrium, whereas fluoride channels have the advantage of more rapid fluoride removal that does not depend on a proton gradient.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim. It may be too vague to check against evidence.

    Interpretationreasoning

    Defluorination chemistry is only a part of the challenge in this field.

    “Furthermore, we argue here that defluorination chemistry is only a part of the challenge in this field.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim. It may be too vague to check against evidence.

    Interpretationreasoning

    Acquiring a deep understanding of fundamental microbial physiologies, in particular fluoride stress responses, can help better harness ancient fluoride resistance mechanisms to address organofluorine biodegradation or biosynthesis.

    “By acquiring a deep understanding of the fundamental microbial physiologies — in particular the fluoride stress responses — that support biodegradation or biosynthesis of organofluorine molecules, we can better harness ancient fluoride resistance mechanisms to address this very contemporary biochemical problem.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    Pseudomonas sp. HXF1 calcium carbonate precipitate can sequester fluoride in the form of CaF2 and Ca5(PO4)3F and diminish fluoride in groundwater.

    “One recent study showed that calcium carbonate precipitate generated by Pseudomonas sp. HXF1 could sequester fluoride in the form of CaF2 and Ca5(PO4)3F and diminish fluoride in groundwater127.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [127] Wang, Z., Su, J. F., Hu, X. F., Ali, A. & Wu, Z. Z. Isolation of biosynthetic crystals by microbially induced calcium carbonate precipitation and their utilization for fluoride removal from groundwater. J. Hazard. Mater. 406, 124748 (2021). source

  • Probably not a substantial claim. The paper may give no reason why it holds.

    Premisenone given

    There is a measurable background rate of non-enzymatic fluorophosphate hydrolysis.

    “However, there is a measurable background rate of non-enzymatic fluorophosphate hydrolysis and so more stable, but inexpensive, fluoride salts like BF4− could be efficacious in this regard.”
    Quote in the paperNot a substantial claim

  • It may state two separate claims as one.

    Premisecitation

    Synthetic proteins that inhibit fluoride channels have been developed but have not been tested in biological systems, and no such natural regulatory mechanism has been identified.

    “Although synthetic proteins that inhibit fluoride channels have been developed123–125, they have not been tested in biological systems, and no such natural regulatory mechanism has been identified.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [123] Stockbridge, R. B., Koide, A., Miller, C. & Koide, S. Proof of dual-topology architecture of Fluc F- channels with monobody blockers. Nat. Commun. 5, 5120 (2014). source
    • cites [124] Turman, D. L. & Stockbridge, R. B. Mechanism of single- and double-sided inhibition of dual topology fluoride channels by synthetic monobodies. J. Gen. Physiol. 149, 511–522 (2017). source
    • cites [125] McIlwain, B. C., Newstead, S. & Stockbridge, R. B. Cork-in-bottle occlusion of fluoride ion channels by crystallization chaperones. Structure 26, 635–639 e1 (2018). source
59 of 59

  • The paper relies on this without support.

    Microbial processes are more easily applied in scenarios with dilute PFAS that preclude technologies relying on PFAS capture and concentration.

    “since microbial processes are more easily applied in scenarios with dilute PFAS that preclude technologies that rely on PFAS capture and concentration.”

  • The paper relies on this without support.

    Bioremediation would be cheaper and more effective than physico-chemical remediation in some circumstances if suitable biological systems can be identified or engineered.

    “Bioremediation would be cheaper and more effective than physico-chemical remediation in some circumstances if suitable biological systems can be identified or engineered.”

  • The paper relies on this without support.

    Biologically-generated replacement chemicals could be designed to have less toxicity and greater biodegradability.

    “Likewise, biologically-generated replacement chemicals could be designed to have less toxicity and greater biodegradability.”

  • The paper relies on this without support.

    PFAS utilization will continue for the foreseeable future.

    “PFAS utilization will continue for the foreseeable future.”

  • The paper relies on this without support.

    Fluoride cannot passively diffuse across the membrane.

    “Because fluoride cannot passively diffuse across the membrane, if this reaction occurs in the cytoplasm, fluoride will accumulate intracellularly.”

  • The paper relies on this without support.

    C–F bond cleavage by any mechanism releases fluorine as a fluoride anion.

    “Some commercial PFAS molecules contain 15 or more fluorines, and due to this atom’s electronegativity, C–F bond cleavage by any mechanism releases fluorine as a fluoride anion.”

  • The paper relies on this without support.

    The medium pH acidifies in dense bacterial cultures.

    “especially as the medium pH acidifies, which is typical with dense bacterial cultures.”

  • The paper relies on this without support.

    There are thousands of enzymes per cell.

    “We have measured enzymatic C–F bond cleavage in one instance to be as fast as 10 bonds cleaved per second per enzyme (and there are thousands of enzymes per cell).”
8 of 8

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 3

  1. Marais, J. S. C. The isolation of the toxic principle “potassium cymonate” from “Gifblaar” Dichapetalum cymosum. Onderstepoort J. Vet. Sci. Anim. Ind. 18, 203–206 (1943).
  2. Walsh, C. Fluorinated substrate-analogs - routes of metabolism and selective toxicity. Adv. Enzymol. Relat. Areas Mol. Biol. 55, 197–289 (1983).
  3. Smith, F. A. Overview of fluorides in everyday life. in Fluorides: Effects in Vegetation, Animals, and Humans (eds. Shupe, J. L., Peterson, H. B. & Leone, N. C.) 7–19 (Paragon Press, Inc., Salt Lake City, UT, 1983).

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Related

Metadata

Authors
Stockbridge, R. B., & Wackett, L. P.
Affiliations
  • University of Michigan (US)
  • University of Minnesota (US)
Corresponding author
  • Stockbridge, Randy B.
  • Wackett, Lawrence P.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2024-05-30
Volume
15
Issue
1
Pages
4593-4593
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-024-49018-1
PMC
PMC11139923
OpenAlex
W4399181105
Semantic Scholar
201950658930be11daff73885148ad8e6cfeb3e1
Cited by
80
References
131
Citations by year
2026: 42 · 2025: 30 · 2024: 8
FWCI
2.34
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • U.S. Department of Health & Human Services | National Institutes of Health (R35 GM128768)
  • MnDRIVE Industry and the Environment Program
Topics
  • Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
  • Physical Sciences › Chemistry › Organic Chemistry › Fluorine in Organic Chemistry
  • Physical Sciences › Environmental Science › Water Science and Technology › Fluoride Effects and Removal
Keywords
fluoride resistance, per- and polyfluoroalkyl substances, fluorinated pesticides, bioengineering
MeSH terms
Bacteria, Biodegradation, Environmental, Fluorides, Hydrocarbons, Fluorinated, Halogenation, Bioengineering

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