{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,11]],"date-time":"2026-06-11T19:06:00Z","timestamp":1781204760505,"version":"3.54.1"},"reference-count":57,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2025,5,7]],"date-time":"2025-05-07T00:00:00Z","timestamp":1746576000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health National Institute of Allergy and Infectious Disease (NIAID)","doi-asserted-by":"publisher","award":["R01 AI116946"],"award-info":[{"award-number":["R01 AI116946"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health National Institute of Allergy and Infectious Disease (NIAID)","doi-asserted-by":"publisher","award":["R01 AI164682"],"award-info":[{"award-number":["R01 AI164682"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Helicobacter pylori is a motile bacterial pathogen that causes severe gastric diseases. H. pylori motility and chemotaxis are key colonization factors. Motility and chemotaxis are studied in many microbes, including H. pylori, using soft agar assays. In these assays, bacteria are inoculated into low-percentage agar and expand in a motility- and chemotaxis-dependent manner. H. pylori similarly expands in soft agar, but, if a plate was inoculated at multiple points, the expanded H. pylori colonies did not merge and left gaps. The basis of these gaps was unknown. We report here that gap formation was not affected by media components such as nutrient and agar concentrations, nor did it require chemotaxis, but it did rely on quorum sensing. To broaden our understanding of this H. pylori property, an H. pylori Tn7 transposon library was screened for mutants that lost gap formation. Fourteen mutants were identified, with transposon sites mapped to genes encoding outer membrane proteins, cysteine-rich proteins, phosphatidyl glycerophosphate synthase, an endorestriction nuclease, and several hypothetical proteins. Our results suggest that H. pylori may use specific proteins to avoid contact with other H. pylori, a behavior that may relate to previous observations that different H. pylori strains do not mix populations in stomach glands.<\/jats:p>","DOI":"10.3390\/microorganisms13051087","type":"journal-article","created":{"date-parts":[[2025,5,7]],"date-time":"2025-05-07T11:46:19Z","timestamp":1746618379000},"page":"1087","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Genetic Basis of Gap Formation Between Migrating Helicobacter pylori Colonies in Soft Agar Assays"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0450-6610","authenticated-orcid":false,"given":"Yasmine","family":"Elshenawi","sequence":"first","affiliation":[{"name":"Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA 95064, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5917-2785","authenticated-orcid":false,"given":"Skander","family":"Hathroubi","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA 95064, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuai","family":"Hu","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA 95064, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5891-4559","authenticated-orcid":false,"given":"Xiaolin","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA 95064, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6265-7401","authenticated-orcid":false,"given":"Karen M.","family":"Ottemann","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, CA 95064, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"ra50","DOI":"10.1126\/scisignal.2000724","article-title":"Origins and Diversification of a Complex Signal Transduction System in Prokaryotes","volume":"3","author":"Wuichet","year":"2010","journal-title":"Sci. Signal."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"6973","DOI":"10.1073\/pnas.86.18.6973","article-title":"Migration of Bacteria in Semisolid Agar","volume":"86","author":"Wolfe","year":"1989","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1016\/j.bpj.2011.06.023","article-title":"Migration of Chemotactic Bacteria in Soft Agar: Role of Gel Concentration","volume":"101","author":"Croze","year":"2011","journal-title":"Biophys. J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1099\/mic.0.062877-0","article-title":"A Supplemented Soft Agar Chemotaxis Assay Demonstrates the Helicobacter pylori Chemotactic Response to Zinc and Nickel","volume":"159","author":"Sanders","year":"2013","journal-title":"Microbiology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1016\/j.bpj.2009.04.018","article-title":"Repulsion and Metabolic Switches in the Collective Behavior of Bacterial Colonies","volume":"97","author":"Sekowska","year":"2009","journal-title":"Biophys. J."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Espeso, D.R., Mart\u00ednez-Garc\u00eda, E., De Lorenzo, V., and Go\u00f1i-Moreno, \u00c1. (2016). Physical Forces Shape Group Identity of Swimming Pseudomonas putida Cells. Front. Microbiol., 7.","DOI":"10.3389\/fmicb.2016.01437"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1146\/annurev.micro.112408.134109","article-title":"Kin Discrimination and Cooperation in Microbes","volume":"65","author":"Strassmann","year":"2011","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Tipping, M.J., and Gibbs, K.A. (2019). Peer Pressure from a Proteus mirabilis Self-Recognition System Controls Participation in Cooperative Swarm Motility. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1007885"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3892","DOI":"10.1128\/JB.00975-08","article-title":"The Dienes Phenomenon: Competition and Territoriality in Swarming Proteus mirabilis","volume":"191","author":"Budding","year":"2009","journal-title":"J. Bacteriol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1700","DOI":"10.1038\/ismej.2014.246","article-title":"Extracellular Matrix Structure Governs Invasion Resistance in Bacterial Biofilms","volume":"9","author":"Nadell","year":"2015","journal-title":"ISME J."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Fung, C., Tan, S., Nakajima, M., Skoog, E.C., Camarillo-Guerrero, L.F., Klein, J.A., Lawley, T.D., Solnick, J.V., Fukami, T., and Amieva, M.R. (2019). High-Resolution Mapping Reveals That Microniches in the Gastric Glands Control Helicobacter pylori Colonization of the Stomach. PLoS Biol., 17.","DOI":"10.1371\/journal.pbio.3000231"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2016","DOI":"10.1128\/IAI.68.4.2016-2023.2000","article-title":"Helicobacter pylori Possesses Two CheY Response Regulators and a Histidine Kinase Sensor, CheA, Which Are Essential for Chemotaxis and Colonization of the Gastric Mucosa","volume":"68","author":"Foynes","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e00406-23","DOI":"10.1128\/jb.00406-23","article-title":"Helicobacter pylori cheV1 Mutants Recover Semisolid Agar Migration Due to Loss of a Previously Uncharacterized Type IV Filament Membrane Alignment Complex Homolog","volume":"206","author":"Sagoo","year":"2024","journal-title":"J. Bacteriol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1038\/s41572-023-00431-8","article-title":"Helicobacter pylori Infection","volume":"9","author":"Malfertheiner","year":"2023","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1056\/NEJMoa001999","article-title":"Helicobacter pylori Infection and the Development of Gastric Cancer","volume":"345","author":"Uemura","year":"2001","journal-title":"N. Engl. J. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1038\/nrc2857","article-title":"Helicobacter pylori: Gastric Cancer and Beyond","volume":"10","author":"Polk","year":"2010","journal-title":"Nat. Rev. Cancer"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Hu, Q., Zhang, Y., Zhang, X., and Fu, K. (2016). Gastric Mucosa-Associated Lymphoid Tissue Lymphoma and Helicobacter pylori Infection: A Review of Current Diagnosis and Management. Biomark. Res., 4.","DOI":"10.1186\/s40364-016-0068-1"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Spagnuolo, R., Scarlata, G.G.M., Paravati, M.R., Abenavoli, L., and Luzza, F. (2024). Change in Diagnosis of Helicobacter pylori Infection in the Treatment-Failure Era. Antibiotics, 13.","DOI":"10.3390\/antibiotics13040357"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1038\/nrgastro.2017.57","article-title":"Helicobacter pylori Infection and Antibiotic Resistance: A WHO High Priority?","volume":"14","author":"Dang","year":"2017","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2140","DOI":"10.1016\/j.cgh.2024.03.008","article-title":"Barriers to Community-Based Eradication of Helicobacter pylori Infection","volume":"22","author":"Kumar","year":"2024","journal-title":"Clin. Gastroenterol. Hepatol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1984","DOI":"10.1128\/IAI.70.4.1984-1990.2002","article-title":"Helicobacter pylori Uses Motility for Initial Colonization and To Attain Robust Infection","volume":"70","author":"Ottemann","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1128\/IAI.73.2.803-811.2005","article-title":"Chemotaxis Plays Multiple Roles during Helicobacter pylori Animal Infection","volume":"73","author":"Terry","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.mib.2017.11.019","article-title":"Colonization, Localization, and Inflammation: The Roles of H. pylori Chemotaxis in Vivo","volume":"41","author":"Johnson","year":"2018","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e01705-16","DOI":"10.1128\/mBio.01705-16","article-title":"Spatial and Temporal Shifts in Bacterial Biogeography and Gland Occupation during the Development of a Chronic Infection","volume":"7","author":"Keilberg","year":"2016","journal-title":"mBio"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e00283-23","DOI":"10.1128\/mbio.00283-23","article-title":"FliL Functions in Diverse Microbes to Negatively Modulate Motor Output via Its N-Terminal Region","volume":"14","author":"Liu","year":"2023","journal-title":"mBio"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"14648","DOI":"10.1073\/pnas.93.25.14648","article-title":"Cag, a Pathogenicity Island of Helicobacter pylori, Encodes Type I-Specific and Disease-Associated Virulence Factors","volume":"93","author":"Censini","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1038\/41483","article-title":"The Complete Genome Sequence of the Gastric Pathogen Helicobacter pylori","volume":"388","author":"Tomb","year":"1997","journal-title":"Nature"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1053\/j.gastro.2010.06.047","article-title":"Tolerance Rather Than Immunity Protects from Helicobacter pylori\u2013Induced Gastric Preneoplasia","volume":"140","author":"Arnold","year":"2011","journal-title":"Gastroenterology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1386","DOI":"10.1016\/S0016-5085(97)70155-0","article-title":"A Standardized Mouse Model of Helicobacter pylori Infection: Introducing the Sydney Strain","volume":"112","author":"Lee","year":"1997","journal-title":"Gastroenterology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e00098-11","DOI":"10.1128\/mBio.00098-11","article-title":"ChePep Controls Helicobacter pylori Infection of the Gastric Glands and Chemotaxis in the Epsilonproteobacteria","volume":"2","author":"Howitt","year":"2011","journal-title":"mBio"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2493","DOI":"10.1099\/00221287-147-9-2493","article-title":"Chemotaxis in the Human Gastric Pathogen Helicobacter pylori: Different Roles for CheW and the Three CheV Paralogues, and Evidence for CheV2 Phosphorylation","volume":"147","author":"Pittman","year":"2001","journal-title":"Microbiology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1181","DOI":"10.1099\/mic.0.021857-0","article-title":"A Fixed-Time Diffusion Analysis Method Determines That the Three Chev Genes of Helicobacter pylori Differentially Affect Motility","volume":"155","author":"Lowenthal","year":"2009","journal-title":"Microbiology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"5877","DOI":"10.1128\/IAI.70.10.5877-5881.2002","article-title":"Two Predicted Chemoreceptors of Helicobacter pylori Promote Stomach Infection","volume":"70","author":"Andermann","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1820","DOI":"10.1128\/IAI.73.3.1820-1827.2005","article-title":"Colonization and Inflammation Deficiencies in Mongolian Gerbils Infected by Helicobacter pylori Chemotaxis Mutants","volume":"73","author":"McGee","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1563","DOI":"10.1128\/JB.00071-16","article-title":"The Helicobacter pylori CZB Cytoplasmic Chemoreceptor TlpD Forms an Autonomous Polar Chemotaxis Signaling Complex That Mediates a Tactic Response to Oxidative Stress","volume":"198","author":"Collins","year":"2016","journal-title":"J. Bacteriol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7926","DOI":"10.1128\/JB.186.23.7926-7935.2004","article-title":"Global Transposon Mutagenesis and Essential Gene Analysis of Helicobacter pylori","volume":"186","author":"Salama","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"7527","DOI":"10.1128\/AEM.69.12.7527-7530.2003","article-title":"Chemoattraction of Vibrio fischeri to Serine, Nucleosides, and N-Acetylneuraminic Acid, a Component of Squid Light-Organ Mucus","volume":"69","author":"Wolfe","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1038\/s41564-018-0314-4","article-title":"Pneumococcal Quorum Sensing Drives an Asymmetric Owner\u2013Intruder Competitive Strategy during Carriage via the Competence Regulon","volume":"4","author":"Shen","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1078\/1438-4221-00204","article-title":"Role of the AlpAB Proteins and Lipopolysaccharide in Adhesion of Helicobacter pylori to Human Gastric Tissue","volume":"292","author":"Odenbreit","year":"2002","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3782","DOI":"10.1128\/IAI.00364-09","article-title":"Outer Membrane Protein Expression Profile in Helicobacter pylori Clinical Isolates","volume":"77","author":"Odenbreit","year":"2009","journal-title":"Infect. Immun."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"3106","DOI":"10.1128\/IAI.01275-10","article-title":"Helicobacter pylori AlpA and AlpB Bind Host Laminin and Influence Gastric Inflammation in Gerbils","volume":"79","author":"Senkovich","year":"2011","journal-title":"Infect. Immun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1016\/j.anaerobe.2011.03.020","article-title":"Analysis of Outer Membrane Vesicle Protein Involved in Biofilm Formation of Helicobacter pylori","volume":"17","author":"Yonezawa","year":"2011","journal-title":"Anaerobe"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"e00729-16","DOI":"10.1128\/JB.00729-16","article-title":"Diversification of the AlpB Outer Membrane Protein of Helicobacter pylori Affects Biofilm Formation and Cellular Adhesion","volume":"199","author":"Yonezawa","year":"2017","journal-title":"J. Bacteriol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1099\/jmm.0.45551-0","article-title":"Role of the Helicobacter pylori Outer-Membrane Proteins AlpA and AlpB in Colonization of the Guinea Pig Stomach","volume":"53","author":"Durrani","year":"2004","journal-title":"J. Med. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1537","DOI":"10.1046\/j.1365-2958.1999.01300.x","article-title":"Genetic and Functional Characterization of the alpAB Gene Locus Essential for the Adhesion of Helicobacter pylori to Human Gastric Tissue","volume":"31","author":"Odenbreit","year":"1999","journal-title":"Mol. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"6242","DOI":"10.1074\/jbc.M611178200","article-title":"Functional and Intracellular Signaling Differences Associated with the Helicobacter pylori  AlpAB Adhesin from Western and East Asian Strains","volume":"282","author":"Lu","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Hathroubi, S., Hu, S., and Ottemann, K.M. (2020). Genetic Requirements and Transcriptomics of Helicobacter pylori Biofilm Formation on Abiotic and Biotic Surfaces. NPJ Biofilms Microbiomes, 6.","DOI":"10.1038\/s41522-020-00167-3"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1002\/prca.201400176","article-title":"Alteration of the Helicobacter pylori Membrane Proteome in Response to Changes in Environmental Salt Concentration","volume":"9","author":"Voss","year":"2015","journal-title":"Proteom. Clin. Appl."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"103374","DOI":"10.1016\/j.jprot.2019.05.002","article-title":"Effect of Environmental Salt Concentration on the Helicobacter pylori Exoproteome","volume":"202","author":"Caston","year":"2019","journal-title":"J. Proteom."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"3638","DOI":"10.1128\/JB.182.13.3638-3643.2000","article-title":"Evidence for a Signaling System in Helicobacter pylori: Detection of a luxS-Encoded Autoinducer","volume":"182","author":"Joyce","year":"2000","journal-title":"J. Bacteriol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"6109","DOI":"10.1128\/JB.00246-07","article-title":"The Quorum-Sensing Molecule Autoinducer 2 Regulates Motility and Flagellar Morphogenesis in Helicobacter pylori","volume":"189","author":"Rader","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2445","DOI":"10.1099\/mic.0.049353-0","article-title":"Helicobacter pylori Perceives the Quorum-Sensing Molecule AI-2 as a Chemorepellent via the Chemoreceptor TlpB","volume":"157","author":"Rader","year":"2011","journal-title":"Microbiology"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Yang, H., Huang, X., Zhang, X., Zhang, X., Xu, X., She, F., and Wen, Y. (2022). AI-2 Induces Urease Expression Through Downregulation of Orphan Response Regulator HP1021 in Helicobacter pylori. Front. Med., 9.","DOI":"10.3389\/fmed.2022.790994"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"e00379-15","DOI":"10.1128\/mBio.00379-15","article-title":"Chemorepulsion from the Quorum Signal Autoinducer-2 Promotes Helicobacter pylori Biofilm Dispersal","volume":"6","author":"Anderson","year":"2015","journal-title":"mBio"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"e12778","DOI":"10.1111\/hel.12778","article-title":"AI-2 represses CagA expression and bacterial adhesion, attenuating the Helicobacter pylori-induced inflammatory response of gastric epithelial cells","volume":"26","author":"Wen","year":"2021","journal-title":"Helicobacter"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"7801","DOI":"10.1073\/pnas.1400782111","article-title":"Cheating by Type 3 Secretion System-Negative Pseudomonas aeruginosa during Pulmonary Infection","volume":"111","author":"Czechowska","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Rizvanov, A.A., Haertl\u00e9, T., Bogomolnaya, L., and Talebi Bezmin Abadi, A. (2019). Helicobacter pylori and Its Antibiotic Heteroresistance: A Neglected Issue in Published Guidelines. Front. Microbiol., 10.","DOI":"10.3389\/fmicb.2019.01796"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/5\/1087\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:28:52Z","timestamp":1760030932000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/5\/1087"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,7]]},"references-count":57,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["microorganisms13051087"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13051087","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,7]]}}}