{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T23:45:05Z","timestamp":1790207105976,"version":"4.1.0"},"reference-count":61,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2021,6,25]],"date-time":"2021-06-25T00:00:00Z","timestamp":1624579200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The present paper is divided into two parts. The first part focuses on the role of Clostridioides difficile in the accumulation of genes associated with antimicrobial resistance and then the transmission of them to other pathogenic bacteria occupying the same human intestinal niche. The second part describes an in silico analysis of the genomes of C. difficile available in GenBank, with regard to the presence of mobile genetic elements and antimicrobial resistance genes. The diversity of the C. difficile genome is discussed, and the current status of resistance of the organisms to various antimicrobial agents is reviewed. The role of transposons associated with antimicrobial resistance is appraised; the importance of plasmids associated with antimicrobial resistance is discussed, and the significance of bacteriophages as a potential shuttle for antimicrobial resistance genes is presented. In the in silico study, 1101 C. difficile genomes were found to harbor mobile genetic elements; Tn6009, Tn6105, CTn7 and Tn6192, Tn6194 and IS256 were the ones more frequently identified. The genes most commonly harbored therein were: ermB, blaCDD, vanT, vanR, vanG and vanS. Tn6194 was likely associated with resistance to erythromycin, Tn6192 and CTn7 with resistance to the \u03b2-lactams and vancomycin, IS256 with resistance to aminoglycoside and Tn6105 to vancomycin.<\/jats:p>","DOI":"10.3390\/microorganisms9071383","type":"journal-article","created":{"date-parts":[[2021,6,25]],"date-time":"2021-06-25T11:07:40Z","timestamp":1624619260000},"page":"1383","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Clostridioides difficile as a Dynamic Vehicle for the Dissemination of Antimicrobial-Resistance Determinants: Review and In Silico Analysis"],"prefix":"10.3390","volume":"9","author":[{"given":"Philip","family":"Kartalidis","sequence":"first","affiliation":[{"name":"Department of Clinical and Laboratory Research, Faculty of Medicine, School of Health Sciences, University of Thessaly, 41110 Larissa, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anargyros","family":"Skoulakis","sequence":"additional","affiliation":[{"name":"Department of Clinical and Laboratory Research, Faculty of Medicine, School of Health Sciences, University of Thessaly, 41110 Larissa, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2819-2089","authenticated-orcid":false,"given":"Katerina","family":"Tsilipounidaki","sequence":"additional","affiliation":[{"name":"Department of Clinical and Laboratory Research, Faculty of Medicine, School of Health Sciences, University of Thessaly, 41110 Larissa, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zoi","family":"Florou","sequence":"additional","affiliation":[{"name":"Department of Clinical and Laboratory Research, Faculty of Medicine, School of Health Sciences, University of Thessaly, 41110 Larissa, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Efthymia","family":"Petinaki","sequence":"additional","affiliation":[{"name":"Department of Clinical and Laboratory Research, Faculty of Medicine, School of Health Sciences, University of Thessaly, 41110 Larissa, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"George C.","family":"Fthenakis","sequence":"additional","affiliation":[{"name":"Veterinary Faculty, University of Thessaly, 43100 Karditsa, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.anaerobe.2016.06.008","article-title":"Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O\u2019Toole 1935) Pr\u00e9vot 1938","volume":"40","author":"Lawson","year":"2016","journal-title":"Anaerobe"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1007\/s10096-019-03539-6","article-title":"Clostridium difficile infection: Review","volume":"38","author":"Czepiel","year":"2019","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2299","DOI":"10.1128\/iai.56.9.2299-2306.1988","article-title":"Actin-specific ADP-ribosyltransferase produced by a Clostridium difficile strain","volume":"56","author":"Popoff","year":"1988","journal-title":"Infect. Immun."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"S6","DOI":"10.1016\/S1995-7645(14)60197-8","article-title":"Clostridium difficile infection: A review of the literature","volume":"7","author":"Khan","year":"2014","journal-title":"Asian Pac. J. Trop. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1111\/j.1469-0691.2012.03853.x","article-title":"European Society of Clinical Microbiology and Infectious Diseases Study Group for Clostridium difficile (ESGCD) Clostridium difficile infection in the community: A zoonotic disease?","volume":"18","author":"Hensgens","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"267","DOI":"10.3390\/antibiotics4030267","article-title":"Antimicrobial resistance and reduced susceptibility in Clostridium difficile: Potential consequences for induction, treatment, and recurrence of C. difficile infection","volume":"4","author":"Baines","year":"2015","journal-title":"Antibiotics"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1186\/s13756-020-00815-5","article-title":"Antimicrobial resistance in Clostridioides (Clostridium) difficile derived from humans: A systematic review and meta-analysis","volume":"9","author":"Sholeh","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_8","first-page":"23","article-title":"Recent advances in the understanding of antibiotic resistance in Clostridium difficile infection","volume":"3","author":"Spigaglia","year":"2016","journal-title":"Ther. Adv. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1128\/CMR.00127-14","article-title":"Diversity and evolution in the genome of Clostridium difficile","volume":"28","author":"Knight","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1038\/ng1830","article-title":"The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome","volume":"38","author":"Sebaihia","year":"2006","journal-title":"Nat. Genet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1193","DOI":"10.1099\/jmm.0.030452-0","article-title":"Reannotation of the genome sequence of Clostridium difficile strain 630","volume":"60","author":"Monot","year":"2011","journal-title":"J. Med. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2125","DOI":"10.1128\/JB.00122-12","article-title":"Draft genome sequence of the nontoxigenic Clostridium difficile strain CD37","volume":"194","author":"Brouwer","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/1757-4749-6-4","article-title":"The genome of Clostridium difficile","volume":"24","author":"Darling","year":"2014","journal-title":"Gut Pathog."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"269","DOI":"10.4161\/gmic.1.4.11870","article-title":"In-depth genetic analysis of Clostridium difficile PCR-ribotype 027 strains reveals high genome fluidity including point mutations and inversions","volume":"1","author":"Stabler","year":"2010","journal-title":"Gut Microbes"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2033","DOI":"10.1007\/s000180200003","article-title":"The clostridial mobilisable transposons","volume":"59","author":"Adams","year":"2002","journal-title":"Cell Mol. Life Sci."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Brouwer, M.S., Warburton, P.J., Roberts, A.P., Mullany, P., and Allan, E. (2011). Genetic organisation, mobility and predicted functions of genes on integrated, mobile genetic elements in sequenced strains of Clostridium difficile. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0023014"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/bs.ampbs.2014.08.002","article-title":"The impact of horizontal gene transfer on the biology of Clostridium difficile","volume":"65","author":"Roberts","year":"2014","journal-title":"Adv. Microbiol. Physiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"8","DOI":"10.4161\/mge.19297","article-title":"Clostridium difficile reveals a related set of conjugative transposons carrying a variety of accessory genes","volume":"2","author":"Brouwer","year":"2012","journal-title":"Mob. Genet. Elem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/0378-1119(96)00511-2","article-title":"A group II intron in a conjugative transposon from the gram-positive bacterium, Clostridium difficile","volume":"174","author":"Mullany","year":"1996","journal-title":"Gene"},{"key":"ref_20","first-page":"e000296","article-title":"An in silico survey of Clostridioides difficile extrachromosomal elements","volume":"5","author":"Hornung","year":"2019","journal-title":"Microb. Genom."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1998","DOI":"10.1128\/JCM.02250-16","article-title":"Update on antimicrobial resistance in Clostridium difficile: Resistance mechanisms and antimicrobial susceptibility testing","volume":"55","author":"Peng","year":"2017","journal-title":"J. Clin. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2227","DOI":"10.1093\/jac\/dkr292","article-title":"European Study Group on Clostridium difficile (ESGCD). Multidrug resistance in European Clostridium difficile clinical isolates","volume":"66","author":"Spigaglia","year":"2011","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"8414257","DOI":"10.1155\/2018\/8414257","article-title":"Clostridium difficile infections: A global overview of drug sensitivity and resistance mechanisms","volume":"2018","author":"Banawas","year":"2018","journal-title":"BioMed Res. Int."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1128\/AAC.31.7.1039","article-title":"Genetic characterization of a Clostridium difficile erythromycin-clindamycin resistance determinant that is transferable to Staphylococcus aureus","volume":"31","author":"Hachler","year":"1987","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1093\/jac\/35.2.305","article-title":"Transfer of macrolide-lincosamide-streptogramin B (MLS) resistance in Clostridium difficile is linked to a gene homologous with toxin A and is mediated by a conjugative transposon, Tn5398","volume":"35","author":"Mullany","year":"1995","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2717","DOI":"10.1099\/00221287-147-10-2717","article-title":"Genomic analysis of the erythromycin resistance element Tn5398 from Clostridium difficile","volume":"147","author":"Farrow","year":"2001","journal-title":"Microbiology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"7527","DOI":"10.1073\/pnas.0914322107","article-title":"Evolutionary dynamics of Clostridium difficile over short and long time scales","volume":"107","author":"He","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1089\/mdr.2014.0015","article-title":"Inter- and intraspecies transfer of a Clostridium difficile conjugative transposon conferring resistance to MLSB","volume":"20","author":"Wasels","year":"2014","journal-title":"Microb. Drug Resis."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Goh, S., Hussain, H., Chang, B.J., Emmett, W., Riley, T.V., and Mullany, P. (2013). phage \u03c6c2 mediates transduction of tn6215, encoding erythromycin resistance, between Clostridium difficile strains. mBio, 4.","DOI":"10.1128\/mBio.00840-13"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1080\/2159256X.2015.1006111","article-title":"Integration of erm(B)-containing elements through large chromosome fragment exchange in Clostridium difficile","volume":"5","author":"Wasels","year":"2015","journal-title":"Mob. Genet. Elem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"102290","DOI":"10.1016\/j.anaerobe.2020.102290","article-title":"Genomic basis of antimicrobial resistance in non-toxigenic Clostridium difficile in Southeast Asia","volume":"66","author":"Imwattana","year":"2020","journal-title":"Anaerobe"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Dingle, K.E., Didelot, X., Quan, T.P., Eyre, D.W., Stoesser, N., Marwick, C.A., Coia, J., Brown, D., Buchanan, S., and Ijaz, U.Z. (2019). Role for tetracycline selection in recent evolution of agriculture-associated Clostridium difficile PCR Ribotype 078. mBio, 10.","DOI":"10.1128\/mBio.02790-18"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2994","DOI":"10.3389\/fmicb.2018.02994","article-title":"Genomic study of a Clostridium difficile multidrug resistant outbreak-related clone reveals novel determinants of resistance","volume":"6","author":"Isidro","year":"2018","journal-title":"Fr. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.ijantimicag.2012.08.011","article-title":"Antimicrobial susceptibility and resistance mechanisms of clinical Clostridium difficile from a Chinese tertiary hospital","volume":"41","author":"Dong","year":"2013","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.resmic.2014.12.005","article-title":"Mobile genetic elements in Clostridium difficile and their role in genome function","volume":"166","author":"Mullany","year":"2015","journal-title":"Res. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"20954","DOI":"10.2807\/1560-7917.ES2014.19.45.20954","article-title":"Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011","volume":"19","author":"Knetsch","year":"2014","journal-title":"EuroSurveillance"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1128\/AAC.00957-07","article-title":"Tetracycline resistance gene tet(W) in the pathogenic bacterium Clostridium difficile","volume":"52","author":"Spigaglia","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Corver, J., Bakker, D., Brouwer, M.S., Harmanus, C., Hensgens, M.P., Roberts, A.P., Lipman, L.J., Kuijper, E.J., and van Leeuwen, H.C. (2012). Analysis of a Clostridium difficile PCR ribotype 078 100 kilobase island reveals the presence of a novel transposon, Tn6164. BMC Microbiol., 12.","DOI":"10.1186\/1471-2180-12-130"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1139\/w2012-002","article-title":"Distribution of the vanG-like gene cluster in Clostridium difficile clinical isolates","volume":"58","author":"Ammam","year":"2012","journal-title":"Can. J. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1111\/mmi.12299","article-title":"The functional vanGCd cluster of Clostridium difficile does not confer vancomycin resistance","volume":"89","author":"Ammam","year":"2013","journal-title":"Mol. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Knight, D.R., Androga, G.O., Ballard, S.A., Howden, B.P., and Riley, T.V. (2016). A phenotypically silent vanB2 operon carried on a Tn1549-like element in Clostridium difficile. mSphere, 1.","DOI":"10.1128\/mSphere.00177-16"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1261\/rna.1371409","article-title":"Identification of 8-methyladenosine as the modification catalyzed by the radical SAM methyltransferase Cfr that confers antibiotic resistance in bacteria","volume":"15","author":"Giessing","year":"2009","journal-title":"RNA"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2530","DOI":"10.1128\/AAC.44.9.2530-2533.2000","article-title":"Identification of a plasmid-borne chloramphenicol-florfenicol resistance gene in Staphylococcus sciuri","volume":"44","author":"Schwarz","year":"2000","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.resmic.2017.12.003","article-title":"The cfr and cfr-like multiple resistance genes","volume":"169","author":"Vester","year":"2018","journal-title":"Res. Microbiol."},{"key":"ref_45","unstructured":"Roberts, M. (2019, October 08). Mechanisms of MLS Resistance. Available online: http:\/\/faculty.washington.edu\/marilynr\/ermwebA.pdf."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1128\/AAC.04082-14","article-title":"Clostridium difficile isolates with high linezolid MICs harbor the multiresistance gene cfr","volume":"59","author":"Cercenado","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2476","DOI":"10.1128\/AAC.04893-14","article-title":"Nomenclature and functionality of the so-called cfr gene from Clostridium difficile","volume":"59","author":"Schwarz","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1016\/j.ijantimicag.2017.03.013","article-title":"A cfr-like gene cfr(C) conferring linezolid resistance is common in Clostridium difficile","volume":"50","author":"Candela","year":"2017","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Stojkovi\u0107, V., Ulate, M.F., Hidalgo-Villeda, F., Aguilar, E., Monge-Cascante, C., Pizarro-Guajardo, M., Tsai, K., Tzoc, E., Camorlinga, M., and Paredes-Sabja, D. (2019). cfr(B), cfr(C), and a new cfr-like gene, cfr(E), in Clostridium difficile strains recovered across Latin America. Antimicrob. Agents Chemother., 64.","DOI":"10.1128\/AAC.01074-19"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.1128\/AAC.32.8.1213","article-title":"Molecular cloning and genetic analysis of a chloramphenicol acetyltransferase determinant from Clostridium difficile","volume":"32","author":"Wren","year":"1998","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"4877","DOI":"10.1093\/nar\/17.12.4877","article-title":"Nucleotide sequence of a chloramphenicol acetyl transferase gene from Clostridium difficile","volume":"17","author":"Wren","year":"1989","journal-title":"Nucleic Acids Res."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1563","DOI":"10.1128\/AAC.42.7.1563","article-title":"Chloramphenicol resistance in Clostridium difficile is encoded on Tn4453 transposons that are closely related to Tn4451 from Clostridium perfringens","volume":"42","author":"Lyras","year":"1998","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Sandhu, B.K., Edwards, A.N., Anderson, S.E., Woods, E.C., and McBride, S.M. (2019). Regulation and anaerobic function of the Clostridioides difficile beta-lactamase. Antimicrob. Agents Chemother., 64.","DOI":"10.1128\/AAC.01496-19"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"598","DOI":"10.1038\/s41467-020-14382-1","article-title":"Plasmid-mediated metronidazole resistance in Clostridioides difficile","volume":"11","author":"Boekhoud","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1038\/nrg3962","article-title":"Horizontal gene transfer: Building the web of life","volume":"16","author":"Soucy","year":"2015","journal-title":"Nat. Rev. Genet."},{"key":"ref_56","first-page":"173","article-title":"Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer","volume":"19","author":"Penders","year":"2016","journal-title":"Fr. Microbiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1093\/femsle\/fnx208","article-title":"Plasmids can transfer to Clostridium difficile CD37 and 630deltaerm both by a DNase resistant conjugation-like mechanism and a DNase sensitive mechanism","volume":"364","author":"Khodadoost","year":"2017","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1093\/jac\/dky420","article-title":"Clostridioides difficile: A potential source of NpmA in the clinical environment","volume":"74","author":"Marsh","year":"2019","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Toth, M., Stewart, N.K., Smith, C., and Vakulenko, S.B. (2018). Intrinsic class D \u03b2-lactamases of Clostridium difficile. mBio, 9.","DOI":"10.1128\/mBio.01803-18"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.plasmid.2015.04.006","article-title":"Extrachromosomal and integrated genetic elements in Clostridium difficile","volume":"80","author":"Amy","year":"2015","journal-title":"Plasmid"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.3390\/genes6041347","article-title":"Disruption of the gut microbiome: Clostridium difficile infection and the threat of antibiotic resistance","volume":"6","author":"Johanesen","year":"2015","journal-title":"Genes"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/7\/1383\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:24:01Z","timestamp":1760163841000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/7\/1383"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,25]]},"references-count":61,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2021,7]]}},"alternative-id":["microorganisms9071383"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9071383","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,25]]}}}