{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,23]],"date-time":"2026-08-23T17:08:17Z","timestamp":1787504897580,"version":"build-2736575974"},"reference-count":47,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2024,3,26]],"date-time":"2024-03-26T00:00:00Z","timestamp":1711411200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Science and Technology Project of the Education Department of Hunan Province","award":["22B0189"],"award-info":[{"award-number":["22B0189"]}]},{"name":"Science and Technology Innovative Research Team in Higher Educational Institutions of Hunan Province","award":["22B0189"],"award-info":[{"award-number":["22B0189"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Multi-drug resistance of bacteria producing extended-spectrum \u03b2-lactamase (ESBL) is a public health challenge. Thus, this study aimed to investigate the antimicrobial susceptibility of ESBL-producing Escherichia coli (ESBL-EC) in Hunan Province, China. A total of 1366 fecal samples were collected from pig, chicken, and cattle farms over a six-year period, which were assessed using strain isolation, 16S rRNA identification, polymerase chain reaction, drug sensitivity testing, whole-genome sequencing, and bioinformatics analysis. The results showed an overall prevalence of 6.66% for ESBL-EC strains, with ESBL positivity extents for pigs, chickens, and cattle isolates at 6.77%, 6.54%, and 12.5%, respectively. Most ESBL-EC isolates were resistant to cefotaxime, tetracycline, and trimethoprim-sulfamethoxazole; however, all the isolates were susceptible to meropenem, with relatively low resistance to amikacin and tigecycline. Various multi-locus sequence types with different origins and similar affinities were identified, with ST155 (n = 16) being the most common subtype. Several types of resistance genes were identified among the 91 positive strains, with beta-lactamase blaCTX-M-55 being the most common ESBL genotype. IncFIB was the predominant plasmid type. Widespread use of antibiotics in animal farming may increase antibiotic resistance, posing a serious threat to the health of farmed animals and, thus, to human food security and health.<\/jats:p>","DOI":"10.3390\/microorganisms12040653","type":"journal-article","created":{"date-parts":[[2024,3,26]],"date-time":"2024-03-26T13:16:41Z","timestamp":1711459001000},"page":"653","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Characterization of Extended-Spectrum \u03b2-Lactamase-Producing Escherichia coli in Animal Farms in Hunan Province, China"],"prefix":"10.3390","volume":"12","author":[{"given":"Ning","family":"Xiao","sequence":"first","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yujuan","family":"Li","sequence":"additional","affiliation":[{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongguang","family":"Lin","sequence":"additional","affiliation":[{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"},{"name":"Institute of Biopharmaceutical and Health Engineering, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen 518055, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Yang","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gang","family":"Xiao","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zonghan","family":"Jiang","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yunqiang","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenxin","family":"Chen","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pengcheng","family":"Zhou","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiliang","family":"Sun","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4877-8199","authenticated-orcid":false,"given":"Jiyun","family":"Li","sequence":"additional","affiliation":[{"name":"College of Veterinary Medicine, Hunan Agricultural University, Changsha 410128, China"},{"name":"Hunan Engineering Technology Research Center of Veterinary Drugs, Hunan Agricultural University, Changsha 410128, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,3,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Breijyeh, Z., Jubeh, B., and Karaman, R. (2020). Resistance of Gram-Negative Bacteria to Current Antibacterial Agents and Approaches to Resolve It. Molecules, 25.","DOI":"10.3390\/molecules25061340"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Sun, C., Cui, M., Zhang, S., Liu, D., Fu, B., Li, Z., Bai, R., Wang, Y., Wang, H., and Song, L. (2020). Genomic Epidemiology of Animal-Derived Tigecycline-Resistant Escherichia coli across China Reveals Recent Endemic Plasmid-Encoded Tet(X4) Gene. Commun. Biol., 3.","DOI":"10.1038\/s42003-020-01148-0"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Bourgard, C., Rodr\u00edguez-Hern\u00e1ndez, D., Rudenko, A., Rutgersson, C., Palm, M., Larsson, D.G.J., Farewell, A., Gr\u00f8tli, M., and Sunnerhagen, P. (2022). Development of Dicationic Bisguanidine-Arylfuran Derivatives as Potent Agents against Gram-Negative Bacteria. Antibiotics, 11.","DOI":"10.3390\/antibiotics11081115"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"118136","DOI":"10.1016\/j.envpol.2021.118136","article-title":"Emergence of Colistin Resistance Genes (Mcr-1) in Escherichia coli among Widely Distributed Wild Ungulates","volume":"291","author":"Torres","year":"2021","journal-title":"Environ. Pollut."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.ijantimicag.2015.09.014","article-title":"Antibiotic Combination Therapy Can Select for Broad-Spectrum Multidrug Resistance in Pseudomonas aeruginosa","volume":"47","author":"Vestergaard","year":"2016","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1038\/ja.2015.68","article-title":"Development of a Multiplex PCR System and Its Application in Detection of blaSHV, blaTEM, blaCTX-M-1, blaCTX-M-9 and blaOXA-1 Group Genes in Clinical Klebsiella pneumoniae and Escherichia coli Strains","volume":"68","author":"Ogutu","year":"2015","journal-title":"J. Antibiot."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.1128\/JCM.36.5.1357-1360.1998","article-title":"Nosocomial Outbreak of Klebsiella pneumoniae Producing SHV-5 Extended-Spectrum Beta-Lactamase, Originating from a Contaminated Ultrasonography Coupling Gel","volume":"36","author":"Gaillot","year":"1998","journal-title":"J. Clin. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1086\/313719","article-title":"Epidemiology of Ciprofloxacin Resistance and Its Relationship to Extended-Spectrum Beta-Lactamase Production in Klebsiella pneumoniae Isolates Causing Bacteremia","volume":"30","author":"Paterson","year":"2000","journal-title":"Clin. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1080\/14656566.2021.1904891","article-title":"Escalating Antimicrobial Resistance among Enterobacteriaceae: Focus on Carbapenemases","volume":"22","author":"Lynch","year":"2021","journal-title":"Expert Opin. Pharmacother."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1111\/tri.12984","article-title":"Changing Trends in the Aetiology, Treatment and Outcomes of Bloodstream Infection Occurring in the First Year after Solid Organ Transplantation: A Single-Centre Prospective Cohort Study","volume":"30","author":"Oriol","year":"2017","journal-title":"Transpl. Int."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"107009","DOI":"10.1289\/EHP5251","article-title":"Inter-Host Transmission of Carbapenemase-Producing Escherichia coli among Humans and Backyard Animals","volume":"127","author":"Li","year":"2019","journal-title":"Environ. Health Perspect."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Kim, H., Kim, Y.A., Seo, Y.H., Lee, H., and Lee, K. (2021). Prevalence and Molecular Epidemiology of Extended-Spectrum-\u03b2-Lactamase (ESBL)-Producing Escherichia coli from Multiple Sectors of Poultry Industry in Korea. Antibiotics, 10.","DOI":"10.3390\/antibiotics10091050"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1046\/j.1198-743x.2001.00330.x","article-title":"Evolution and Epidemiology of Extended-Spectrum Beta-Lactamases (ESBLs) and ESBL-Producing Microorganisms","volume":"7","author":"Gniadkowski","year":"2001","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1128\/CMR.18.4.657-686.2005","article-title":"Extended-Spectrum Beta-Lactamases: A Clinical Update","volume":"18","author":"Paterson","year":"2005","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_15","first-page":"344","article-title":"The Antibiotic Resistance Crisis","volume":"40","author":"Ventola","year":"2015","journal-title":"Pharm. Ther."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/s41564-018-0151-5","article-title":"A High-Frequency Phenotypic Switch Links Bacterial Virulence and Environmental Survival in Acinetobacter baumannii","volume":"3","author":"Chin","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"35465","DOI":"10.1038\/srep35465","article-title":"An Anti-Infective Synthetic Peptide with Dual Antimicrobial and Immunomodulatory Activities","volume":"6","author":"Silva","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1016\/j.jiph.2023.02.021","article-title":"A Parallel and Silent Emerging Pandemic: Antimicrobial Resistance (AMR) amid COVID-19 Pandemic","volume":"16","author":"Rehman","year":"2023","journal-title":"J. Infect. Public Health"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"105638","DOI":"10.1016\/j.envint.2020.105638","article-title":"Maternal Antibiotic Concentrations in Pregnant Women in Shanghai and Their Determinants: A Biomonitoring-Based Prospective Study","volume":"138","author":"Zeng","year":"2020","journal-title":"Environ. Int."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"104858","DOI":"10.1016\/j.prevetmed.2019.104858","article-title":"Knowledge, Attitudes and Practices Relating to Antibiotic Use and Antibiotic Resistance among Backyard Pig Farmers in Rural Shandong Province, China","volume":"175","author":"Dyar","year":"2020","journal-title":"Prev. Vet. Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1186\/s13756-019-0672-6","article-title":"Antibiotic Use in Chicken Farms in Northwestern China","volume":"9","author":"Xu","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/978-3-319-64371-7_14","article-title":"Strain Diversity and the Evolution of Antibiotic Resistance","volume":"1019","author":"Borrell","year":"2017","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e14","DOI":"10.1017\/S0950268822001509","article-title":"Integrated Surveillance of Extended-Spectrum Beta-Lactamase (ESBL)-Producing Salmonella and Escherichia coli from Humans and Animal Species Raised for Human Consumption in Canada from 2012 to 2017","volume":"151","author":"Primeau","year":"2022","journal-title":"Epidemiol. Infect."},{"key":"ref_24","first-page":"mgen000951","article-title":"The Risk of Pig and Chicken Farming for Carriage and Transmission of Escherichia coli Containing Extended-Spectrum Beta-Lactamase (ESBL) and Mobile Colistin Resistance (Mcr) Genes in Thailand","volume":"9","author":"Sudatip","year":"2023","journal-title":"Microb. Genom."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"285","DOI":"10.3343\/alm.2021.41.3.285","article-title":"Prevalence and Molecular Epidemiology of Extended-Spectrum-\u03b2-Lactamase (ESBL)-Producing Escherichia coli from Multiple Sectors of the Swine Industry in Korea: A Korean Nationwide Monitoring Program for a One Health Approach to Combat Antimicrobial Resistance","volume":"41","author":"Kim","year":"2021","journal-title":"Ann. Lab. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1294","DOI":"10.1002\/vms3.773","article-title":"Prevalence and Antimicrobial Susceptibility of CTX-M-Type-Producing Escherichia coli from a Wildlife Zoo in China","volume":"8","author":"Zeng","year":"2022","journal-title":"Vet. Med. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/j.mayocpiqo.2023.07.010","article-title":"Diagnostic Yield of 16S Ribosomal Ribonucleic Acid Gene-Based Targeted Metagenomic Sequencing for Evaluation of Pleural Space Infection: A Prospective Study","volume":"7","author":"Samhouri","year":"2023","journal-title":"Mayo Clin. Proc. Innov. Qual. Outcomes"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"7086","DOI":"10.1128\/AAC.01363-15","article-title":"Emergence of Raoultella ornithinolytica Coproducing IMP-4 and KPC-2 Carbapenemases in China","volume":"59","author":"Zheng","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Lin, H., Chen, W., Zhou, R., Yang, J., Wu, Y., Zheng, J., Fei, S., Wu, G., Sun, Z., and Li, J. (2022). Characteristics of the Plasmid-Mediated Colistin-Resistance Gene Mcr-1 in Escherichia coli Isolated from a Veterinary Hospital in Shanghai. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.1002827"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Chen, W., Liu, Z., Lin, H., Yang, J., Liu, T., Zheng, J., Long, X., Sun, Z., Li, J., and Chen, X. (2022). Occurrence of blaNDM-1-Positive Providencia Spp. in a Pig Farm of China. Antibiotics, 11.","DOI":"10.3390\/antibiotics11060713"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1737","DOI":"10.1002\/ibd.20966","article-title":"Phylogenetic Analysis of Inflammatory Bowel Disease Associated Escherichia coli and the fimH Virulence Determinant","volume":"15","author":"Sepehri","year":"2009","journal-title":"Inflamm. Bowel Dis."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1089\/cmb.2012.0021","article-title":"SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing","volume":"19","author":"Bankevich","year":"2012","journal-title":"J. Comput. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Treangen, T.J., Ondov, B.D., Koren, S., and Phillippy, A.M. (2014). The Harvest Suite for Rapid Core-Genome Alignment and Visualization of Thousands of Intraspecific Microbial Genomes. Genome Biol., 15.","DOI":"10.1186\/s13059-014-0524-x"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Hu, J., Yang, J., Chen, W., Liu, Z., Zhao, Q., Yang, H., Sun, Z., Chen, X., and Li, J. (2022). Prevalence and Characteristics of Mcr-1-Producing Escherichia coli in Three Kinds of Poultry in Changsha, China. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.840520"},{"key":"ref_35","first-page":"e000192","article-title":"ClermonTyping: An Easy-to-Use and Accurate in Silico Method for Escherichia Genus Strain Phylotyping","volume":"4","author":"Beghain","year":"2018","journal-title":"Microb. Genom."},{"key":"ref_36","first-page":"100220","article-title":"China\u2019s Low-Emission Pathways toward Climate-Neutral Livestock Production for Animal-Derived Foods","volume":"3","author":"Wang","year":"2022","journal-title":"Innovation"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.envint.2017.10.016","article-title":"Review of Antibiotic Resistance in China and Its Environment","volume":"110","author":"Qiao","year":"2018","journal-title":"Environ. Int."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1038\/s43016-022-00470-6","article-title":"Distinct Increase in Antimicrobial Resistance Genes among Escherichia coli during 50 Years of Antimicrobial Use in Livestock Production in China","volume":"3","author":"Yang","year":"2022","journal-title":"Nat. Food"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Liu, Z., Wang, K., Zhang, Y., Xia, L., Zhao, L., Guo, C., Liu, X., Qin, L., and Hao, Z. (2021). High Prevalence and Diversity Characteristics of blaNDM, Mcr, and blaESBLs Harboring Multidrug-Resistant Escherichia coli from Chicken, Pig, and Cattle in China. Front. Cell. Infect. Microbiol., 11.","DOI":"10.3389\/fcimb.2021.755545"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1038\/s41426-018-0033-1","article-title":"Rapid Rise of the ESBL and Mcr-1 Genes in Escherichia coli of Chicken Origin in China, 2008\u20132014","volume":"7","author":"Wu","year":"2018","journal-title":"Emerg. Microbes Infect."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.jinf.2021.06.004","article-title":"Etiology and Prevalence of ESBLs in Adult Community-Onset Urinary Tract Infections in East China: A Prospective Multicenter Study","volume":"83","author":"Quan","year":"2021","journal-title":"J. Infect."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"864080","DOI":"10.3389\/fnut.2022.864080","article-title":"Protective Effects of Intestinal Gallic Acid in Neonatal Dairy Calves Against Extended-Spectrum \u03b2-Lactamase Producing Enteroaggregative Escherichia coli Infection: Modulating Intestinal Homeostasis and Colitis","volume":"9","author":"He","year":"2022","journal-title":"Front. Nutr."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.15212\/ZOONOSES-2023-0011","article-title":"Successful Treatment of Pasteurella Multocida-Related Invasive Infections with a Beta-Lactamase Inhibitor-Sparing Combination Antibiotic Regimen: A Case Series","volume":"3","author":"Mastroianni","year":"2023","journal-title":"Zoonoses"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Xiao, R., Li, Y., Liu, X., Ding, Y., Lai, J., Li, Y., Kang, W., Zou, P., Wang, J., and Du, Y. (2023). Antibiotic Susceptibility of Escherichia coli Isolated from Neonates Admitted to Neonatal Intensive Care Units across China from 2015 to 2020. Front. Cell. Infect. Microbiol., 13.","DOI":"10.3389\/fcimb.2023.1183736"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1007\/s12088-023-01074-9","article-title":"Evaluation of the Lytic Activity of Various Phage Cocktails Against, ESBL-Producer, Non-Producer and Carbapenem-Resistant Escherichia coli Isolates","volume":"63","author":"Yalcin","year":"2023","journal-title":"Indian J. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1894","DOI":"10.1097\/CM9.0000000000000368","article-title":"Spreading of Extended-Spectrum \u03b2-Lactamase-Producing Escherichia coli ST131 and Klebsiella pneumoniae ST11 in Patients with Pneumonia: A Molecular Epidemiological Study","volume":"132","author":"Liu","year":"2019","journal-title":"Chin. Med. J."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"4464","DOI":"10.1128\/AAC.00501-15","article-title":"blaCTX-M-1\/9\/1 Hybrid Genes May Have Been Generated from blaCTX-M-15 on an IncI2 Plasmid","volume":"59","author":"Liu","year":"2015","journal-title":"Antimicrob. Agents Chemother."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/4\/653\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:18:34Z","timestamp":1760105914000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/4\/653"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,26]]},"references-count":47,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,4]]}},"alternative-id":["microorganisms12040653"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms12040653","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,26]]}}}