{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T19:22:05Z","timestamp":1788290525710,"version":"build-2803163510"},"reference-count":69,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,6,7]],"date-time":"2021-06-07T00:00:00Z","timestamp":1623024000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,6,7]],"date-time":"2021-06-07T00:00:00Z","timestamp":1623024000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p><jats:italic>Staphylococcus epidermidis<\/jats:italic> (<jats:italic>S. epidermidis<\/jats:italic>) ATCC 12228 was incubated with 2% polyethylene glycol (PEG)-8 Laurate to yield electricity which was measured by a voltage difference between electrodes. Production of electron was validated by a Ferrozine assay. The anti-<jats:italic>Cutibacterium acnes<\/jats:italic> (<jats:italic>C. acnes<\/jats:italic>) activity of electrogenic <jats:italic>S. epidermidis<\/jats:italic> was assessed in vitro and in vivo. The voltage change (~\u20094.4\u00a0mV) reached a peak 60\u00a0min after pipetting <jats:italic>S. epidermidis<\/jats:italic> plus 2% PEG-8 Laurate onto anodes. The electricity produced by <jats:italic>S. epidermidis<\/jats:italic> caused significant growth attenuation and cell lysis of <jats:italic>C. acnes<\/jats:italic>. Intradermal injection of <jats:italic>C. acnes<\/jats:italic> and <jats:italic>S. epidermidis<\/jats:italic> plus PEG-8 Laurate into the mouse ear considerably suppressed the growth of <jats:italic>C. acnes.<\/jats:italic> This suppressive effect was noticeably reversed when cyclophilin A of <jats:italic>S. epidermidis<\/jats:italic> was inhibited, indicating the essential role of cyclophilin A in electricity production of <jats:italic>S. epidermidis<\/jats:italic> against C<jats:italic>. acnes.<\/jats:italic> In summary, we demonstrate for the first time that skin <jats:italic>S. epidermidis<\/jats:italic>, in the presence of PEG-8 Laurate, can mediate cyclophilin A to elicit an electrical current that has anti-<jats:italic>C. acnes<\/jats:italic> effects. Electricity generated by <jats:italic>S. epidermidis<\/jats:italic> may confer immediate innate immunity in acne lesions to rein in the overgrowth of <jats:italic>C. acnes<\/jats:italic> at the onset of acne vulgaris.<\/jats:p>","DOI":"10.1038\/s41598-021-91398-7","type":"journal-article","created":{"date-parts":[[2021,6,7]],"date-time":"2021-06-07T10:06:06Z","timestamp":1623060366000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Electricity-producing Staphylococcus epidermidis counteracts Cutibacterium acnes"],"prefix":"10.1038","volume":"11","author":[{"given":"Shinta","family":"Marito","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sunita","family":"Keshari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Supitchaya","family":"Traisaeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Do Thi Tra","family":"My","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arun","family":"Balasubramaniam","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Prakoso","family":"Adi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ming-Fa","family":"Hsieh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Deron Raymond","family":"Herr","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chun-Ming","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,6,7]]},"reference":[{"key":"91398_CR1","first-page":"244","volume":"9","author":"EA Grice","year":"2011","unstructured":"Grice, E. A. & Segre, J. A. J. N. r. m. The skin microbiome. 9, 244\u2013253 (2011).","journal-title":"N. r. m. The skin microbiome."},{"key":"91398_CR2","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1038\/nri.2017.7","volume":"17","author":"M Levy","year":"2017","unstructured":"Levy, M., Kolodziejczyk, A. A., Thaiss, C. A. & Elinav, E. Dysbiosis and the immune system. Nat Rev Immunol 17, 219\u2013232. https:\/\/doi.org\/10.1038\/nri.2017.7 (2017).","journal-title":"Nat Rev Immunol"},{"key":"91398_CR3","doi-asserted-by":"publisher","first-page":"1233","DOI":"10.1016\/j.jaci.2016.04.053","volume":"138","author":"B Shi","year":"2016","unstructured":"Shi, B. et al. The skin microbiome is different in pediatric versus adult atopic dermatitis. J Allergy Clin Immunol 138, 1233\u20131236. https:\/\/doi.org\/10.1016\/j.jaci.2016.04.053 (2016).","journal-title":"J Allergy Clin Immunol"},{"key":"91398_CR4","doi-asserted-by":"publisher","unstructured":"Gao, Z., Tseng, C. H., Strober, B. E., Pei, Z. & Blaser, M. J. Substantial alterations of the cutaneous bacterial biota in psoriatic lesions. PLoS ONE 3, https:\/\/doi.org\/10.1371\/journal.pone.0002719 (2008).","DOI":"10.1371\/journal.pone.0002719"},{"key":"91398_CR5","doi-asserted-by":"publisher","first-page":"850","DOI":"10.1101\/gr.131029.111","volume":"22","author":"HH Kong","year":"2012","unstructured":"Kong, H. H. et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res 22, 850\u2013859. https:\/\/doi.org\/10.1101\/gr.131029.111 (2012).","journal-title":"Genome Res"},{"key":"91398_CR6","first-page":"2152","volume":"133","author":"S Fitz-Gibbon","year":"2013","unstructured":"Fitz-Gibbon, S. et al. Propionibacterium acnes strain populations in the human skin microbiome associated with acne. 133, 2152\u20132160 (2013).","journal-title":"Propionibacterium acnes strain populations in the human skin microbiome associated with acne."},{"key":"91398_CR7","doi-asserted-by":"publisher","first-page":"329","DOI":"10.5582\/ddt.2018.01079","volume":"12","author":"I Kanwar","year":"2018","unstructured":"Kanwar, I. et al. Models for acne: A comprehensive study. Drug Discoveries & Therapeutics 12, 329\u2013340. https:\/\/doi.org\/10.5582\/ddt.2018.01079 (2018).","journal-title":"Drug Discoveries & Therapeutics"},{"key":"91398_CR8","doi-asserted-by":"crossref","unstructured":"Kao, M. S. et al. Microbiome precision editing: Using PEG as a selective fermentation initiator against methicillin\u2010resistant Staphylococcus aureus. Biotechnology journal 12 (2017).","DOI":"10.1002\/biot.201600399"},{"key":"91398_CR9","doi-asserted-by":"publisher","first-page":"1870","DOI":"10.3390\/ijms17111870","volume":"17","author":"Y Wang","year":"2016","unstructured":"Wang, Y. et al. A precision microbiome approach using sucrose for selective augmentation of Staphylococcus epidermidis fermentation against Propionibacterium acnes. Int. J. Mol. Sci. 17, 1870 (2016).","journal-title":"Int. J. Mol. Sci."},{"key":"91398_CR10","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1111\/j.1574-6941.2006.00214.x","volume":"59","author":"N Finke","year":"2007","unstructured":"Finke, N., Vandieken, V. & J\u00f8rgensen, B. B. Acetate, lactate, propionate, and isobutyrate as electron donors for iron and sulfate reduction in Arctic marine sediments. Svalbard. FEMS Microbiology Ecology 59, 10\u201322 (2007).","journal-title":"Svalbard. FEMS Microbiology Ecology"},{"key":"91398_CR11","first-page":"e02983","volume":"83","author":"C Chen","year":"2017","unstructured":"Chen, C., Shen, Y., An, D. & Voordouw, G. Use of acetate, propionate, and butyrate for reduction of nitrate and sulfate and methanogenesis in microcosms and bioreactors simulating an oil reservoir. Appl. Environ. Microbiol. 83, e02983-e12916 (2017).","journal-title":"Appl. Environ. Microbiol."},{"key":"91398_CR12","doi-asserted-by":"crossref","unstructured":"Sorokin, D. Y., Detkova, E. & Muyzer, G. Propionate and butyrate dependent bacterial sulfate reduction at extremely haloalkaline conditions and description of Desulfobotulus alkaliphilus sp. nov. Extremophiles 14, 71\u201377 (2010).","DOI":"10.1007\/s00792-009-0288-5"},{"key":"91398_CR13","doi-asserted-by":"publisher","first-page":"32","DOI":"10.1016\/j.aca.2019.05.007","volume":"1076","author":"G Pankratova","year":"2019","unstructured":"Pankratova, G., Hederstedt, L. & Gorton, L. Extracellular electron transfer features of Gram-positive bacteria. Anal. Chim. Acta 1076, 32\u201347 (2019).","journal-title":"Anal. Chim. Acta"},{"key":"91398_CR14","doi-asserted-by":"crossref","unstructured":"Xayarath, B., Alonzo III, F. & Freitag, N. E. Identification of a peptide-pheromone that enhances Listeria monocytogenes escape from host cell vacuoles. PLoS pathogens 11 (2015).","DOI":"10.1371\/journal.ppat.1004707"},{"key":"91398_CR15","doi-asserted-by":"publisher","first-page":"10163","DOI":"10.1021\/es200834b","volume":"45","author":"S Matsuda","year":"2011","unstructured":"Matsuda, S., Liu, H., Kato, S., Hashimoto, K. & Nakanishi, S. Negative faradaic resistance in extracellular electron transfer by anode-respiring Geobacter sulfurreducens cells. Environ. Sci. Technol. 45, 10163\u201310169 (2011).","journal-title":"Environ. Sci. Technol."},{"key":"91398_CR16","doi-asserted-by":"crossref","unstructured":"Pankratova, G., Leech, D. n., Gorton, L. & Hederstedt, L. Extracellular electron transfer by the Gram-positive bacterium Enterococcus faecalis. Biochemistry 57, 4597\u20134603 (2018).","DOI":"10.1021\/acs.biochem.8b00600"},{"key":"91398_CR17","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1038\/s41586-018-0498-z","volume":"562","author":"SH Light","year":"2018","unstructured":"Light, S. H. et al. A flavin-based extracellular electron transfer mechanism in diverse Gram-positive bacteria. Nature 562, 140 (2018).","journal-title":"Nature"},{"key":"91398_CR18","doi-asserted-by":"crossref","unstructured":"Carpenter, J. M. et al. Structure and redox properties of the diheme electron carrier cytochrome c4 from Pseudomonas aeruginosa. Journal of inorganic biochemistry 203, 110889 (2020).","DOI":"10.1016\/j.jinorgbio.2019.110889"},{"key":"91398_CR19","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1016\/j.bbrc.2010.01.135","volume":"393","author":"C Bonfils","year":"2010","unstructured":"Bonfils, C. et al. Cyclophilin A as negative regulator of apoptosis by sequestering cytochrome c. Biochem. Biophys. Res. Commun. 393, 325\u2013330 (2010).","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"91398_CR20","doi-asserted-by":"publisher","first-page":"29826","DOI":"10.1074\/jbc.M101822200","volume":"276","author":"SP Lee","year":"2001","unstructured":"Lee, S. P. et al. Cyclophilin a binds to peroxiredoxins and activates its peroxidase activity. J. Biol. Chem. 276, 29826\u201329832 (2001).","journal-title":"J. Biol. Chem."},{"key":"91398_CR21","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1146\/annurev-micro-092611-150104","volume":"66","author":"DR Lovley","year":"2012","unstructured":"Lovley, D. R. Electromicrobiology. Annu. Rev. Microbiol. 66, 391\u2013409 (2012).","journal-title":"Annu. Rev. Microbiol."},{"key":"91398_CR22","doi-asserted-by":"publisher","first-page":"521","DOI":"10.1128\/IAI.01125-12","volume":"81","author":"MS Roset","year":"2013","unstructured":"Roset, M. S., Fern\u00e1ndez, L. G., DelVecchio, V. G. & Briones, G. Intracellularly induced cyclophilins play an important role in stress adaptation and virulence of Brucella abortus. Infect. Immun. 81, 521\u2013530 (2013).","journal-title":"Infect. Immun."},{"key":"91398_CR23","doi-asserted-by":"publisher","first-page":"1535","DOI":"10.1007\/s00253-018-9484-5","volume":"103","author":"X Liu","year":"2019","unstructured":"Liu, X. et al. Biological synthesis of high-conductive pili in aerobic bacterium Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 103, 1535\u20131544 (2019).","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"91398_CR24","doi-asserted-by":"publisher","first-page":"12138","DOI":"10.1021\/acs.analchem.9b03176","volume":"91","author":"W Wang","year":"2019","unstructured":"Wang, W. et al. Bacterial Extracellular Electron Transfer Occurs in Mammalian Gut. Anal. Chem. 91, 12138\u201312141 (2019).","journal-title":"Anal. Chem."},{"key":"91398_CR25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.bioelechem.2018.08.002","volume":"125","author":"MY Kim","year":"2019","unstructured":"Kim, M. Y. et al. Metabolic shift of Klebsiella pneumoniae L17 by electrode-based electron transfer using glycerol in a microbial fuel cell. Bioelectrochemistry 125, 1\u20137 (2019).","journal-title":"Bioelectrochemistry"},{"key":"91398_CR26","doi-asserted-by":"publisher","first-page":"3517","DOI":"10.1128\/AAC.00673-08","volume":"52","author":"M Giladi","year":"2008","unstructured":"Giladi, M. et al. Microbial growth inhibition by alternating electric fields. Antimicrob. Agents Chemother. 52, 3517\u20133522 (2008).","journal-title":"Antimicrob. Agents Chemother."},{"key":"91398_CR27","doi-asserted-by":"publisher","first-page":"319","DOI":"10.3390\/v8110319","volume":"8","author":"J Fertey","year":"2016","unstructured":"Fertey, J. et al. Pathogens inactivated by low-energy-electron irradiation maintain antigenic properties and induce protective immune responses. Viruses 8, 319 (2016).","journal-title":"Viruses"},{"key":"91398_CR28","doi-asserted-by":"publisher","first-page":"1561","DOI":"10.1016\/j.vaccine.2018.02.014","volume":"36","author":"L Bayer","year":"2018","unstructured":"Bayer, L., Fertey, J., Ulbert, S. & Grunwald, T. Immunization with an adjuvanted low-energy electron irradiation inactivated respiratory syncytial virus vaccine shows immunoprotective activity in mice. Vaccine 36, 1561\u20131569 (2018).","journal-title":"Vaccine"},{"key":"91398_CR29","doi-asserted-by":"publisher","first-page":"1376","DOI":"10.1111\/j.1365-2672.2007.03374.x","volume":"103","author":"A Valle","year":"2007","unstructured":"Valle, A. et al. Effects of low electric current (LEC) treatment on pure bacterial cultures. J. Appl. Microbiol. 103, 1376\u20131385 (2007).","journal-title":"J. Appl. Microbiol."},{"key":"91398_CR30","first-page":"63","volume":"6","author":"MJ Angelaalincy","year":"2018","unstructured":"Angelaalincy, M. J. et al. Biofilm engineering approaches for improving the performance of microbial fuel cells and bioelectrochemical systems. 6, 63 (2018).","journal-title":"Biofilm engineering approaches for improving the performance of microbial fuel cells and bioelectrochemical systems."},{"key":"91398_CR31","first-page":"1","volume":"10","author":"A Balasubramaniam","year":"2020","unstructured":"Balasubramaniam, A. et al. Repurposing INCI-registered compounds as skin prebiotics for probiotic Staphylococcus epidermidis against UV-B. 10, 1\u201310 (2020).","journal-title":"Repurposing INCI-registered compounds as skin prebiotics for probiotic Staphylococcus epidermidis against UV-B."},{"key":"91398_CR32","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1186\/s12864-016-2489-5","volume":"17","author":"GJ Christensen","year":"2016","unstructured":"Christensen, G. J. et al. Antagonism between Staphylococcus epidermidis and Propionibacterium acnes and its genomic basis. BMC Genomics 17, 152 (2016).","journal-title":"BMC Genomics"},{"key":"91398_CR33","doi-asserted-by":"publisher","first-page":"5295","DOI":"10.1021\/jm9008295","volume":"52","author":"S Ni","year":"2009","unstructured":"Ni, S. et al. Discovering potent small molecule inhibitors of cyclophilin A using de novo drug design approach. J. Med. Chem. 52, 5295\u20135298 (2009).","journal-title":"J. Med. Chem."},{"key":"91398_CR34","first-page":"1092","volume":"8","author":"A Balasubramaniam","year":"2020","unstructured":"Balasubramaniam, A. et al. Skin Bacteria Mediate Glycerol Fermentation to Produce Electricity and Resist UV-B. 8, 1092 (2020).","journal-title":"Skin Bacteria Mediate Glycerol Fermentation to Produce Electricity and Resist UV-B."},{"key":"91398_CR35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s40064-015-1476-7","volume":"4","author":"S Halder","year":"2015","unstructured":"Halder, S. et al. Alteration of Zeta potential and membrane permeability in bacteria: a study with cationic agents. Springerplus 4, 1\u201314 (2015).","journal-title":"Springerplus"},{"key":"91398_CR36","doi-asserted-by":"publisher","unstructured":"Keshari, S. et al. Butyric Acid from Probiotic Staphylococcus epidermidis in the Skin Microbiome Down-Regulates the Ultraviolet-Induced Pro-Inflammatory IL-6 Cytokine via Short-Chain Fatty Acid Receptor. Int J Mol Sci 20, https:\/\/doi.org\/10.3390\/ijms20184477 (2019).","DOI":"10.3390\/ijms20184477"},{"key":"91398_CR37","doi-asserted-by":"crossref","unstructured":"Marito, S., Keshari, S. & Huang, C.-M. J. I. J. o. M. S. PEG-8 Laurate Fermentation of Staphylococcus epidermidis Reduces the Required Dose of Clindamycin Against Cutibacterium acnes. 21, 5103 (2020).","DOI":"10.3390\/ijms21145103"},{"key":"91398_CR38","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1186\/1471-2180-10-98","volume":"10","author":"ST Read","year":"2010","unstructured":"Read, S. T., Dutta, P., Bond, P. L., Keller, J. & Rabaey, K. Initial development and structure of biofilms on microbial fuel cell anodes. BMC Microbiol. 10, 98 (2010).","journal-title":"BMC Microbiol."},{"key":"91398_CR39","doi-asserted-by":"crossref","unstructured":"Goodarzi, A., Mozafarpoor, S., Bodaghabadi, M. & Mohamadi, M. The potential of probiotics for treating acne vulgaris: A review of literature on acne and microbiota. Dermatologic Therapy (2020).","DOI":"10.1111\/dth.13279"},{"key":"91398_CR40","doi-asserted-by":"publisher","first-page":"411","DOI":"10.1007\/s00253-013-5394-8","volume":"98","author":"Y Wang","year":"2014","unstructured":"Wang, Y. et al. Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris. Appl. Microbiol. Biotechnol. 98, 411\u2013424 (2014).","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"91398_CR41","doi-asserted-by":"publisher","first-page":"34045","DOI":"10.1039\/C4RA03489A","volume":"4","author":"JA Modestra","year":"2014","unstructured":"Modestra, J. A. & Mohan, S. V. Bio-electrocatalyzed electron efflux in Gram positive and Gram negative bacteria: an insight into disparity in electron transfer kinetics. RSC Adv. 4, 34045\u201334055 (2014).","journal-title":"RSC Adv."},{"key":"91398_CR42","doi-asserted-by":"crossref","unstructured":"Di Domenico, E. G. et al. Development of electroactive and anaerobic ammonium-oxidizing (anammox) biofilms from digestate in microbial fuel cells. BioMed research international 2015 (2015).","DOI":"10.1155\/2015\/351014"},{"key":"91398_CR43","unstructured":"Liu, R., Zhao, Y., Lu, S. & Huang, Q. Electricity generation from lactate using microbial fuel cell and the distribution characteristics of anode microbial community. Wei sheng wu xue bao= Acta microbiologica Sinica 52, 744\u2013752 (2012)."},{"key":"91398_CR44","doi-asserted-by":"publisher","first-page":"3968","DOI":"10.1073\/pnas.0710525105","volume":"105","author":"E Marsili","year":"2008","unstructured":"Marsili, E. et al. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105, 3968\u20133973. https:\/\/doi.org\/10.1073\/pnas.0710525105 (2008).","journal-title":"Proc Natl Acad Sci U S A"},{"key":"91398_CR45","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1016\/j.biortech.2015.04.080","volume":"190","author":"B Chen","year":"2015","unstructured":"Chen, B. et al. Role of extracellular polymeric substances from Chlorella vulgaris in the removal of ammonium and orthophosphate under the stress of cadmium. Biores. Technol. 190, 299\u2013306 (2015).","journal-title":"Biores. Technol."},{"key":"91398_CR46","doi-asserted-by":"publisher","first-page":"657","DOI":"10.22438\/jeb\/38\/4\/MRN-284","volume":"38","author":"B Hong","year":"2017","unstructured":"Hong, B. et al. Influence of salinity variations on exocellular polysaccharide production, biofilm formation and flocculation in halotolerant bacteria. J. Environ. Biol. 38, 657 (2017).","journal-title":"J. Environ. Biol."},{"key":"91398_CR47","doi-asserted-by":"crossref","unstructured":"Christenson, L. Algal biofilm production and harvesting system for wastewater treatment with biofuels by-products. (2011).","DOI":"10.1016\/j.biotechadv.2011.05.015"},{"key":"91398_CR48","doi-asserted-by":"crossref","unstructured":"Angelaalincy, M. et al. Enhanced extracellular polysaccharide production and self-sustainable electricity generation for PAMFCs by Scenedesmus sp. SB1. ACS omega 2, 3754\u20133765 (2017).","DOI":"10.1021\/acsomega.7b00326"},{"key":"91398_CR49","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1186\/s13068-016-0426-0","volume":"9","author":"O Choi","year":"2016","unstructured":"Choi, O. & Sang, B.-I. Extracellular electron transfer from cathode to microbes: application for biofuel production. Biotechnol. Biofuels 9, 11. https:\/\/doi.org\/10.1186\/s13068-016-0426-0 (2016).","journal-title":"Biotechnol. Biofuels"},{"key":"91398_CR50","doi-asserted-by":"publisher","first-page":"706","DOI":"10.1038\/nrmicro2422","volume":"8","author":"K Rabaey","year":"2010","unstructured":"Rabaey, K. & Rozendal, R. A. Microbial electrosynthesis - revisiting the electrical route for microbial production. Nat Rev Microbiol 8, 706\u2013716. https:\/\/doi.org\/10.1038\/nrmicro2422 (2010).","journal-title":"Nat Rev Microbiol"},{"key":"91398_CR51","doi-asserted-by":"publisher","first-page":"8234","DOI":"10.1128\/AEM.05382-11","volume":"77","author":"GE Pinchuk","year":"2011","unstructured":"Pinchuk, G. E. et al. Pyruvate and lactate metabolism by Shewanella oneidensis MR-1 under fermentation, oxygen limitation, and fumarate respiration conditions. Appl. Environ. Microbiol. 77, 8234\u20138240 (2011).","journal-title":"Appl. Environ. Microbiol."},{"key":"91398_CR52","doi-asserted-by":"publisher","first-page":"63","DOI":"10.3389\/fenrg.2018.00063","volume":"6","author":"MJ Angelaalincy","year":"2018","unstructured":"Angelaalincy, M. J. et al. Biofilm engineering approaches for improving the performance of microbial fuel cells and bioelectrochemical systems. Frontiers in Energy Research 6, 63 (2018).","journal-title":"Frontiers in Energy Research"},{"key":"91398_CR53","doi-asserted-by":"crossref","unstructured":"Pankratova, G., Hederstedt, L. & Gorton, L. J. A. c. a. Extracellular electron transfer features of Gram-positive bacteria. 1076, 32\u201347 (2019).","DOI":"10.1016\/j.aca.2019.05.007"},{"key":"91398_CR54","doi-asserted-by":"publisher","first-page":"855","DOI":"10.1016\/j.jid.2016.11.014","volume":"137","author":"A Schwarz","year":"2017","unstructured":"Schwarz, A., Bruhs, A. & Schwarz, T. The short-chain fatty acid sodium butyrate functions as a regulator of the skin immune system. J. Investig. Dermatol. 137, 855\u2013864 (2017).","journal-title":"J. Investig. Dermatol."},{"key":"91398_CR55","first-page":"1","volume":"17","author":"GJ Christensen","year":"2016","unstructured":"Christensen, G. J. et al. Antagonism between Staphylococcus epidermidis and Propionibacterium acnes and its genomic basis. 17, 1\u201314 (2016).","journal-title":"Antagonism between Staphylococcus epidermidis and Propionibacterium acnes and its genomic basis."},{"key":"91398_CR56","first-page":"411","volume":"98","author":"Y Wang","year":"2014","unstructured":"Wang, Y. et al. Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris. 98, 411\u2013424 (2014).","journal-title":"Staphylococcus epidermidis in the human skin microbiome mediates fermentation to inhibit the growth of Propionibacterium acnes: implications of probiotics in acne vulgaris."},{"key":"91398_CR57","doi-asserted-by":"crossref","unstructured":"Claudel, J.-P. et al. Staphylococcus epidermidis: a potential new player in the physiopathology of acne? 235, 287\u2013294 (2019).","DOI":"10.1159\/000499858"},{"key":"91398_CR58","doi-asserted-by":"crossref","unstructured":"Kim, J. J. D. Review of the innate immune response in acne vulgaris: activation of Toll-like receptor 2 in acne triggers inflammatory cytokine responses. 211, 193\u2013198 (2005).","DOI":"10.1159\/000087011"},{"key":"91398_CR59","doi-asserted-by":"crossref","unstructured":"Hoare, J. I., Rajnicek, A. M., McCaig, C. D., Barker, R. N. & Wilson, H. M. J. J. o. l. b. Electric fields are novel determinants of human macrophage functions. 99, 1141\u20131151 (2016).","DOI":"10.1189\/jlb.3A0815-390R"},{"key":"91398_CR60","first-page":"1","volume":"4","author":"T Nakatsuji","year":"2013","unstructured":"Nakatsuji, T. et al. The microbiome extends to subepidermal compartments of normal skin. 4, 1\u20138 (2013).","journal-title":"The microbiome extends to subepidermal compartments of normal skin."},{"key":"91398_CR61","doi-asserted-by":"crossref","unstructured":"Pouillot, A., Polla, A. & S Polla, B. Iron and iron chelators: a review on potential effects on skin aging. Current aging science 6, 225\u2013231 (2013).","DOI":"10.2174\/18746098112059990037"},{"key":"91398_CR62","doi-asserted-by":"publisher","unstructured":"Pakhomova, O. N., Gregory, B. W., Semenov, I. & Pakhomov, A. G. Two modes of cell death caused by exposure to nanosecond pulsed electric field. PLoS ONE 8, https:\/\/doi.org\/10.1371\/journal.pone.0070278 (2013).","DOI":"10.1371\/journal.pone.0070278"},{"key":"91398_CR63","doi-asserted-by":"publisher","first-page":"3288","DOI":"10.1158\/0008-5472.can-04-0083","volume":"64","author":"ED Kirson","year":"2004","unstructured":"Kirson, E. D. et al. Disruption of cancer cell replication by alternating electric fields. Cancer Res 64, 3288\u20133295. https:\/\/doi.org\/10.1158\/0008-5472.can-04-0083 (2004).","journal-title":"Cancer Res"},{"key":"91398_CR64","doi-asserted-by":"publisher","first-page":"19778","DOI":"10.1038\/srep19778","volume":"6","author":"F Pillet","year":"2016","unstructured":"Pillet, F., Formosa-Dague, C., Baaziz, H., Dague, E. & Rols, M.-P. Cell wall as a target for bacteria inactivation by pulsed electric fields. Sci. Rep. 6, 19778. https:\/\/doi.org\/10.1038\/srep19778 (2016).","journal-title":"Sci. Rep."},{"key":"91398_CR65","doi-asserted-by":"publisher","first-page":"3280","DOI":"10.1073\/pnas.0712331105","volume":"105","author":"JI Yeh","year":"2008","unstructured":"Yeh, J. I., Chinte, U. & Du, S. Structure of glycerol-3-phosphate dehydrogenase, an essential monotopic membrane enzyme involved in respiration and metabolism. Proc Natl Acad Sci U S A 105, 3280\u20133285. https:\/\/doi.org\/10.1073\/pnas.0712331105 (2008).","journal-title":"Proc Natl Acad Sci U S A"},{"key":"91398_CR66","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1016\/j.molcel.2006.06.019","volume":"23","author":"TH Massey","year":"2006","unstructured":"Massey, T. H., Mercogliano, C. P., Yates, J., Sherratt, D. J. & Lowe, J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 23, 457\u2013469. https:\/\/doi.org\/10.1016\/j.molcel.2006.06.019 (2006).","journal-title":"Mol Cell"},{"key":"91398_CR67","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1016\/j.tcb.2003.09.005","volume":"13","author":"R Carballido-Lopez","year":"2003","unstructured":"Carballido-Lopez, R. & Errington, J. A dynamic bacterial cytoskeleton. Trends Cell Biol 13, 577\u2013583. https:\/\/doi.org\/10.1016\/j.tcb.2003.09.005 (2003).","journal-title":"Trends Cell Biol"},{"key":"91398_CR68","doi-asserted-by":"publisher","first-page":"W512","DOI":"10.1093\/nar\/gkm307","volume":"35","author":"CE Felder","year":"2007","unstructured":"Felder, C. E., Prilusky, J., Silman, I. & Sussman, J. L. A server and database for dipole moments of proteins. Nucleic Acids Res 35, W512-521. https:\/\/doi.org\/10.1093\/nar\/gkm307 (2007).","journal-title":"Nucleic Acids Res"},{"key":"91398_CR69","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1016\/s0167-7012(01)00240-8","volume":"45","author":"F Ahimou","year":"2001","unstructured":"Ahimou, F., Paquot, M., Jacques, P., Thonart, P. & Rouxhet, P. G. Influence of electrical properties on the evaluation of the surface hydrophobicity of Bacillus subtilis. J Microbiol Methods 45, 119\u2013126. https:\/\/doi.org\/10.1016\/s0167-7012(01)00240-8 (2001).","journal-title":"J Microbiol Methods"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-91398-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-91398-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-91398-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,3]],"date-time":"2022-12-03T09:22:24Z","timestamp":1670059344000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-91398-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,7]]},"references-count":69,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["91398"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-91398-7","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,7]]},"assertion":[{"value":"10 August 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"12001"}}