{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T23:21:56Z","timestamp":1789428116313,"version":"build-2803163510"},"reference-count":64,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,5,26]],"date-time":"2021-05-26T00:00:00Z","timestamp":1621987200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>Neutrophils, the first line of the host\u2019s defense, use a variety of antimicrobial mechanisms to fight invading pathogens. One of the most crucial is the production of neutrophil extracellular traps (NETs) in the process called NETosis. The unique structure of NETs effectively inhibits the spread of pathogens and ensures their exposure to a high concentration of NET-embedded antimicrobial compounds. NETosis strategy is often used by the host to defend against fungal infection caused by <jats:italic>Candida albicans<\/jats:italic>. In immunocompromised patients, this microorganism is responsible for developing systemic fungal infections (candidiasis). This is correlated with the use of a vast array of virulence factors, leading to the acquisition of specific resistance to host defense factors and available drug therapies. One of the most important features favoring the development of drug resistance is a <jats:italic>C. albicans<\/jats:italic> ability to form biofilms that protect fungal cells mainly through the production of an extracellular matrix (ECM). Among the main ECM-building macromolecules extracellular nucleic acids have been identified and their role is probably associated with the stbilization of the biofilm structure. The complex interactions of immune cells with the thick ECM layer, comprising the first line of contact between these cells and the biofilm structure, are still poorly understood. Therefore, the current studies aimed to assess the release of extracellular nucleic acids by <jats:italic>C. albicans<\/jats:italic> strains at different stages of biofilm formation, and to determine the role of these molecules in triggering the NETosis. We showed for the first time that fungal nucleic acids, purified directly from mature <jats:italic>C. albicans<\/jats:italic> biofilm structure or obtained from the whole fungal cells, have the potential to induce NET release <jats:italic>in vitro<\/jats:italic>. In this study, we considered the involvement of TLR8 and TLR9 in NETosis activation. We showed that DNA and RNA molecules initiated the production of reactive oxygen species (ROS) by activation of the NADPH oxidase complex, essential for ROS-dependent NETosis. Furthermore, analysis of the cell migration showed that the nucleic acids located in the extracellular space surrounding the biofilm may be also effective chemotactic factors, driving the dynamic migration of human neutrophils to the site of ongoing fungal infection.<\/jats:p>","DOI":"10.3389\/fcimb.2021.681030","type":"journal-article","created":{"date-parts":[[2021,5,26]],"date-time":"2021-05-26T06:47:05Z","timestamp":1622011625000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":42,"title":["Extracellular Nucleic Acids Present in the Candida albicans Biofilm Trigger the Release of Neutrophil Extracellular Traps"],"prefix":"10.3389","volume":"11","author":[{"given":"Magdalena","family":"Smolarz","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcin","family":"Zawrotniak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dorota","family":"Satala","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria","family":"Rapala-Kozik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,5,26]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1770","DOI":"10.1128\/EC.00219-06","article-title":"Production of Tyrosol by Candida Albicans Biofilms and Its Role in Quorum Sensing and Biofilm Development","volume":"5","author":"Alem","year":"2006","journal-title":"Eukaryot. Cell"},{"key":"B2","doi-asserted-by":"publisher","first-page":"e101342","DOI":"10.1371\/journal.pone.0101342","article-title":"TLR9 and NF-\u03bab are Partially Involved in Activation of Human Neutrophils by Helicobacter Pylori and Its Purified DNA","volume":"9","author":"Alvarez-Arellano","year":"2014","journal-title":"PLoS One"},{"key":"B3","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1146\/annurev-med-052814-023338","article-title":"Importance of Nucleic Acid Recognition in Inflammation and Autoimmunity","volume":"67","author":"Barrat","year":"2016","journal-title":"Annu. Rev. Med."},{"key":"B4","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1038\/nri2587.A","article-title":"A Cell Biological View of Toll-Like Receptor Function: Regulation Through Compartmentalization","volume":"9","author":"Barton","year":"2009","journal-title":"Nat. Rev. Immunol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"588","DOI":"10.1016\/j.mib.2006.10.003","article-title":"How to Build a Biofilm: A Fungal Perspective","volume":"9","author":"Blankenship","year":"2006","journal-title":"Curr. Opin. Microbiol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1038\/ni.2987","article-title":"Neutrophils Sense Microbial Size and Selectively Release Neutrophil Extracellular Traps in Response to Large Pathogens","volume":"15","author":"Branzk","year":"2015","journal-title":"Nat. Immunol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1532","DOI":"10.1126\/science.1092385","article-title":"Neutrophil Extracellular Traps Kill Bacteria","volume":"303","author":"Brinkmann","year":"2004","journal-title":"Science"},{"key":"B8","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1016\/j.dci.2014.01.003","article-title":"The Effect of \u03b2-Glucan on Formation and Functionality of Neutrophil Extracellular Traps in Carp (Cyprinus Carpio L.)","volume":"44","author":"Brogden","year":"2014","journal-title":"Dev. Comp. Immunol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"4136","DOI":"10.4049\/jimmunol.1202671.An","article-title":"An Extracellular Matrix-Based Mechanism of Rapid Neutrophil Extracellular Trap Formation in Response to","volume":"190","author":"Byrd","year":"2013","journal-title":"J. Immunol."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.3389\/fmed.2018.00028","article-title":"Candida Biofilms: Threats, Challenges, and Promising Strategies","volume":"5","author":"Cavalheiro","year":"2018","journal-title":"Front. Med."},{"key":"B11","doi-asserted-by":"publisher","first-page":"1932","DOI":"10.1172\/JCI112190","article-title":"Activation of the Human Neutrophil Nicotinamide Adenine Dinucleotide Phosphate (NADPH)-Oxidase by Protein Kinase C","volume":"76","author":"Cox","year":"1985","journal-title":"J. Clin. Invest."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/srep07763","article-title":"Extracellular Vesicle-Mediated Export of Fungal RNA","volume":"5","author":"Da Silva","year":"2015","journal-title":"Sci. Rep."},{"key":"B13","doi-asserted-by":"publisher","first-page":"2817","DOI":"10.1073\/pnas.1414055112","article-title":"SK3 Channel and Mitochondrial ROS Mediate NADPH Oxidase-Independent NETosis Induced by Calcium Influx","volume":"112","author":"Douda","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B14","doi-asserted-by":"publisher","first-page":"6386","DOI":"10.4049\/jimmunol.0901640","article-title":"Extracellular DNA: A Major Proinflammatory Component of Pseudomonas Aeruginosa Biofilms","volume":"184","author":"Fuxman Bass","year":"2010","journal-title":"J. Immunol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1080\/21505594.2016.1184385","article-title":"In Vivo Induction of Neutrophil Chemotaxis by Secretory Aspartyl Proteinases of Candida Albicans","volume":"7","author":"Gabrielli","year":"2016","journal-title":"Virulence"},{"key":"B16","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1038\/nchembio.496","article-title":"Activation of the Raf-MEK-ERK Pathway Is Required for Neutrophil Extracellular Trap Formation","volume":"7","author":"Hakkim","year":"2011","journal-title":"Nat. Chem. Biol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1099\/00222615-47-3-253","article-title":"Production of Extracellular Matrix by Candida Albicans Biofilms","volume":"47","author":"Hawser","year":"1998","journal-title":"J. Med. Microbiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"2660","DOI":"10.1182\/blood-2003-04-1078","article-title":"Toll-Like Receptors Stimulate Human Neutrophil Function","volume":"102","author":"Hayashi","year":"2003","journal-title":"Blood"},{"key":"B19","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1038\/s41467-019-13756-4","article-title":"Neutrophil Extracellular Trap-Associated RNA and LL37 Enable Self-Amplifying Inflammation in Psoriasis","volume":"11","author":"Herster","year":"2020","journal-title":"Nat. Commun."},{"key":"B20","doi-asserted-by":"publisher","first-page":"2982","DOI":"10.1128\/AEM.67.7.2982","article-title":"Quorum Sensing in the Dimorphic Fungus Candida Albicans Is Mediated by Farnesol","volume":"67","author":"Hornby","year":"2001","journal-title":"Appl. Environ. Microbiol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"e00797","DOI":"10.1128\/AAC.00797-18","article-title":"Echinocandin Treatment of Candida Albicans Biofilms Enhances Neutrophil Extracellular Trap Formation","volume":"62","author":"Hoyer","year":"2018","journal-title":"Antimicrob. Agents Chemother."},{"key":"B22","doi-asserted-by":"publisher","first-page":"788","DOI":"10.1038\/nature08476","article-title":"STING Regulates Intracellular DNA-Mediated, Type I Interferon-Dependent Innate Immunity","volume":"461","author":"Ishikawa","year":"2009","journal-title":"Nature"},{"key":"B23","doi-asserted-by":"publisher","first-page":"2786","DOI":"10.1093\/nar\/19.10.2786","article-title":"Mono Q Chromatography Permits Recycling of DNA Template and Purification of RNA Transcripts After T7 RNA Polymerase Reaction","volume":"19","author":"Jahn","year":"1991","journal-title":"Nucleic Acids Res."},{"key":"B24","doi-asserted-by":"publisher","first-page":"1026","DOI":"10.1016\/j.jaci.2009.02.015","article-title":"Selective and Direct Activation of Human Neutrophils But Not Eosinophils by Toll-like Receptor 8","volume":"123","author":"Janke","year":"2009","journal-title":"J. Allergy Clin. Immunol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.ppat.1005884","article-title":"The Extracellular Matrix of Candida Albicans Biofilms Impairs Formation of Neutrophil Extracellular Traps","volume":"12","author":"Johnson","year":"2016","journal-title":"PLoS Pathog."},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2014.00461","article-title":"Toll-Like Receptor Signaling Pathways","volume":"5","author":"Kawasaki","year":"2014","journal-title":"Front. Immunol."},{"key":"B27","first-page":"215","article-title":"Cytosolic Nucleic Acid Sensors in Inflammatory and Autoimmune Disorders","volume-title":"International Review of Cell and Molecular Biology","author":"Khan","year":"2019"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1155\/2010\/986596","article-title":"Classification, Mechanisms of Action, and Therapeutic Applications of Inhibitory Oligonucleotides for Toll-Like Receptors (TLR) 7 and 9","volume":"2010","author":"Lenert","year":"2010","journal-title":"Mediators Inflamm."},{"key":"B29","doi-asserted-by":"publisher","first-page":"2101","DOI":"10.1002\/eji.201142143","article-title":"Primary Blood Neutrophils Express a Functional Cell Surface Toll-Like Receptor 9","volume":"43","author":"Lindau","year":"2013","journal-title":"Eur. J. Immunol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/cpr.12579","article-title":"Induction of Neutrophil Extracellular Traps During Tissue Injury: Involvement of STING and Toll-like Receptor 9 Pathways","volume":"52","author":"Liu","year":"2019","journal-title":"Cell Prolif."},{"key":"B31","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/S1471-4914(02)02280-3","article-title":"Molecular Basis of Resistance to Azole Antifungals","volume":"8","author":"Lupetti","year":"2002","journal-title":"Trends Mol. Med."},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2018.00288","article-title":"The Neutrophil\u2019s Choice: Phagocytose vs Make Neutrophil Extracellular Traps","volume":"9","author":"Manfredi","year":"2018","journal-title":"Front. Immunol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"80","DOI":"10.1111\/j.1439-0507.2011.02047.x","article-title":"Addition of DNase Improves the In Vitro Activity of Antifungal Drugs Against Candida Albicans Biofilms","volume":"55","author":"Martins","year":"2012","journal-title":"Mycoses"},{"key":"B34","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1007\/s11046-009-9264-y","article-title":"Presence of Extracellular DNA in the Candida Albicans Biofilm Matrix and its Contribution to Biofilms","volume":"169","author":"Martins","year":"2010","journal-title":"Mycopathologia"},{"key":"B35","doi-asserted-by":"publisher","first-page":"119","DOI":"10.4161\/viru.22913","article-title":"Candida Albicans Pathogenicity","volume":"4","author":"Mayer","year":"2013","journal-title":"Virulence"},{"key":"B36","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1016\/S0958-1669(03)00036-3","article-title":"Gene Transfer Occurs With Enhanced Efficiency in Biofilms and Induces Enhanced Stabilisation of the Biofilm Structure","volume":"14","author":"Molin","year":"2003","journal-title":"Curr. Opin. Biotechnol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.ppat.1000213","article-title":"Extracellular DNA Chelates Cations and Induces Antibiotic Resistance in Pseudomonas Aeruginosa Biofilms","volume":"4","author":"Mulcahy","year":"2008","journal-title":"PLoS Pathog."},{"key":"B38","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1016\/j.mib.2019.06.002","article-title":"Candidalysin: Discovery and Function in Candida Albicans Infections","volume":"52","author":"Naglik","year":"2019","journal-title":"Curr. Opin. Microbiol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"3266","DOI":"10.1099\/mic.0.2008\/022293-0.Quantitative","article-title":"Quantitative Expression of the Candida Albicans Secreted Aspartyl Proteinase Gene Family in Human Oral and Vaginal Candidiasis","volume":"154","author":"Naglik","year":"2008","journal-title":"Microbiology"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-51427-y","article-title":"Self-DNA Release and STING-dependent Sensing Drives Inflammation to Cigarette Smoke in Mice","volume":"9","author":"Nascimento","year":"2019","journal-title":"Sci. Rep."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1604","DOI":"10.1128\/EC.00194-06","article-title":"Function of Candida Albicans Adhesin Hwp1 in Biofilm Formation","volume":"5","author":"Nobile","year":"2006","journal-title":"Eukaryot. Cell"},{"key":"B42","doi-asserted-by":"publisher","first-page":"4664","DOI":"10.1073\/pnas.071404698","article-title":"Purification and Characterization of an Autoregulatory Substance Capable of Regulating the Morphological Transition in Candida Albicans","volume":"98","author":"Oh","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B43","doi-asserted-by":"publisher","first-page":"341","DOI":"10.3109\/1040841X.2013.841639","article-title":"The Role of Extracellular DNA in the Establishment, Maintenance and Perpetuation of Bacterial Biofilms","volume":"41","author":"Okshevsky","year":"2015","journal-title":"Crit. Rev. Microbiol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"7413","DOI":"10.4049\/jimmunol.1000675","article-title":"A Novel Mechanism of Rapid Nuclear Neutrophil Extracellular Trap Formation in Response to Staphylococcus Aureus","volume":"185","author":"Pilsczek","year":"2010","journal-title":"J. Immunol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12866-014-0303-6","article-title":"Extracellular DNA Release Confers Heterogeneity in Candida Albicans Biofilm Formation","volume":"14","author":"Rajendran","year":"2014","journal-title":"BMC Microbiol."},{"key":"B46","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1111\/omi.12206","article-title":"Extracellular Proteinases of Candida Species Pathogenic Yeasts","volume":"33","author":"Rapala-Kozik","year":"2018","journal-title":"Mol. Oral. Microbiol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"18302","DOI":"10.1038\/srep18302","article-title":"Classical ROS-dependent and Early\/Rapid ROS-Independent Release of Neutrophil Extracellular Traps Triggered by Leishmania Parasites","volume":"5","author":"Rochael","year":"2015","journal-title":"Sci. Rep."},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2017.00306","article-title":"Prokaryotic RNA Associated to Bacterial Viability Induces Polymorphonuclear Neutrophil Activation","volume":"7","author":"Rodriguez-Rodrigues","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1177\/0022034516675849","article-title":"A Critical Role for Extracellular DNA in Dental Plaque Formation","volume":"96","author":"Rostami","year":"2016","journal-title":"J.\u00a0Dent. Res."},{"key":"B50","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.chom.2012.05.015","article-title":"Neutrophil Extracellular Traps Mediate a Host Defense Response to Human Immunodeficiency Virus-1","volume":"12","author":"Saitoh","year":"2012","journal-title":"Cell Host Microbe"},{"key":"B51","doi-asserted-by":"publisher","first-page":"1531","DOI":"10.1111\/jam.12483","article-title":"Effects of Extracellular DNA From Candida Albicans and Pneumonia-Related Pathogens on Candida Biofilm Formation and Hyphal Transformation","volume":"116","author":"Sapaar","year":"2014","journal-title":"J.\u00a0Appl. Microbiol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"1053","DOI":"10.1128\/EC.2.5.1053","article-title":"Engineered Control of Cell Morphology In Vivo Reveals Distinct Roles for Yeast and Filamentous Forms of Candida Albicans During Infection","volume":"2","author":"Saville","year":"2003","journal-title":"Eukaryot. Cell"},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1101\/527267","article-title":"The Biofilm Matrix Scaffold of Pseudomonas Species Contains Non-Canonically Base Paired Extracellular DNA and RNA","author":"Seviour","year":"2019","journal-title":"Biochemistry"},{"key":"B54","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1038\/s41416-018-0339-8","article-title":"Mitochondrial DNA in the Tumour Microenvironment Activates Neutrophils and is Associated With Worse Outcomes in Patients With Advanced Epithelial Ovarian Cancer","volume":"120","author":"Singel","year":"2019","journal-title":"Br. J. Cancer"},{"key":"B55","doi-asserted-by":"publisher","first-page":"1702","DOI":"10.1128\/JCM.29.8.1702-1710.1991","article-title":"Genetic Dissimilarity of Commensal Strains of Candida Spp. Carried in Different Anatomical Locations of the Same Healthy Women","volume":"29","author":"Soll","year":"1991","journal-title":"J. Clin. Microbiol"},{"key":"B56","doi-asserted-by":"publisher","first-page":"1325","DOI":"10.2217\/fmb.13.101","article-title":"Mechanisms of Candida Biofilm Drug Resistance","volume":"8","author":"Taff","year":"2013","journal-title":"Future Microbiol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2180-8-187","article-title":"Phenotypic Screening, Transcriptional Profiling, and Comparative Genomic Analysis of an Invasive and non-Invasive Strain of Candida Albicans","volume":"8","author":"Thewes","year":"2008","journal-title":"BMC Microbiol."},{"key":"B58","doi-asserted-by":"publisher","first-page":"e1000639","DOI":"10.1371\/journal.ppat.1000639","article-title":"Neutrophil Extracellular Traps Contain Calprotectin, a Cytosolic Protein Complex Involved in Host Defense Against Candida Albicans","volume":"5","author":"Urban","year":"2009","journal-title":"PLoS Pathog."},{"key":"B59","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1111\/j.1462-5822.2005.00659.x","article-title":"Neutrophil Extracellular Traps Capture and Kill Candida Albicans and Hyphal Forms","volume":"8","author":"Urban","year":"2006","journal-title":"Cell. Microbiol."},{"key":"B60","doi-asserted-by":"publisher","DOI":"10.1126\/science.295.5559.1487","article-title":"Extracellular DNA Required for Bacterial Biofilm Formation","volume":"295","author":"Whitchurch","year":"2002","journal-title":"Science"},{"key":"B61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/mBio.01333-14","article-title":"Novel Entries in a Fungal Biofilm Matrix Encyclopedia","volume":"5","author":"Zarnowski","year":"2014","journal-title":"MBio"},{"key":"B62","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2017.00414","article-title":"Aspartic Proteases and Major Cell Wall Components in Candida Albicans Trigger the Release of Neutrophil Extracellular Traps","volume":"7","author":"Zawrotniak","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.3390\/cells8121611","article-title":"Farnesol, a Quorum-Sensing Molecule of Candida Albicans Triggers the Release of Neutrophil Extracellular Traps","volume":"8","author":"Zawrotniak","year":"2019","journal-title":"Cells"},{"key":"B64","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1038\/nchembio.2518","article-title":"Small-Molecule Inhibition of TLR8 Through Stabilization of Its Resting State","volume":"14","author":"Zhang","year":"2018","journal-title":"Nat. Chem. Biol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2021.681030\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,26]],"date-time":"2021-05-26T06:47:10Z","timestamp":1622011630000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2021.681030\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,26]]},"references-count":64,"alternative-id":["10.3389\/fcimb.2021.681030"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2021.681030","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,26]]},"article-number":"681030"}}