{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T12:26:35Z","timestamp":1784550395324,"version":"3.55.0"},"reference-count":49,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T00:00:00Z","timestamp":1747094400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Natural Science Foundation of China","award":["22378167"],"award-info":[{"award-number":["22378167"]}]},{"name":"National Natural Science Foundation of China","award":["251111310300"],"award-info":[{"award-number":["251111310300"]}]},{"name":"Key Research and Development Program of Henan province","award":["22378167"],"award-info":[{"award-number":["22378167"]}]},{"name":"Key Research and Development Program of Henan province","award":["251111310300"],"award-info":[{"award-number":["251111310300"]}]}],"content-domain":{"domain":["www.mdpi.com"],"crossmark-restriction":true},"short-container-title":["Microorganisms"],"abstract":"<jats:p>To accurately detect internal and environmental cues, bacteria have evolved signal transduction pathways such as two-component systems (TCSs) to reprogram appropriate genetic and physiological functions for adaptation and survival. The MprAB TCS is commonly found in actinobacteria and has been associated with important processes such as mycobacterial virulence, nutrient starvation, and environmental stress, particularly cell envelope stress. However, a comprehensive investigation of the function and response network of the MprAB TCS in corynebacteria remains to be carried out. In this study, we report that the MprAB TCS (previously named CgtSR2) plays a critical role in regulating genes involved in cell envelope remodeling in C. glutamicum. The results indicated that the MprAB TCS directly controls a broad regulon, including cell wall biosynthesis proteins, alternative sigma factors, secreted proteins of unknown function, and the mprAB gene locus itself. Among these, the HtrA-like serine protease confers vancomycin and penicillin resistance. Furthermore, we found that the function of the cell envelope was disrupted during overexpression of mprA, resulting in elongated cell morphology and increased cell membrane permeability, as well as enhanced excretion of L-alanine. In conclusion, our findings provide novel insights into how the conserved MprAB TCS controls cell envelope homeostasis in distant actinobacteria.<\/jats:p>","DOI":"10.3390\/microorganisms13051120","type":"journal-article","created":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T06:40:23Z","timestamp":1747118423000},"page":"1120","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Two-Component MprAB System Regulates the Expression of Genes Involved in Cell Envelope Biosynthesis in Corynebacterium glutamicum"],"prefix":"10.3390","volume":"13","author":[{"given":"Yu","family":"Zou","sequence":"first","affiliation":[{"name":"School of Biotechnology and Key Laboratory of Industrial Biotechnology of Ministry of Education, Jiangnan University, Wuxi 214122, China"},{"name":"National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi 214122, China"},{"name":"Jiangsu Provincial Engineering Research Center for Bioactive Product Processing, Jiangnan University, Wuxi 214122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danni","family":"Huang","sequence":"additional","affiliation":[{"name":"School of Biotechnology and Key Laboratory of Industrial Biotechnology of Ministry of Education, Jiangnan University, Wuxi 214122, China"},{"name":"National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi 214122, China"},{"name":"Jiangsu Provincial Engineering Research Center for Bioactive Product Processing, Jiangnan University, Wuxi 214122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiuxia","family":"Liu","sequence":"additional","affiliation":[{"name":"School of Biotechnology and Key Laboratory of Industrial Biotechnology of Ministry of Education, Jiangnan University, Wuxi 214122, China"},{"name":"National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi 214122, China"},{"name":"Jiangsu Provincial Engineering Research Center for Bioactive Product Processing, Jiangnan University, Wuxi 214122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4815-6832","authenticated-orcid":false,"given":"Yankun","family":"Yang","sequence":"additional","affiliation":[{"name":"School of Biotechnology and Key Laboratory of Industrial Biotechnology of Ministry of Education, Jiangnan University, Wuxi 214122, China"},{"name":"National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi 214122, China"},{"name":"Jiangsu Provincial Engineering Research Center for Bioactive Product Processing, Jiangnan University, Wuxi 214122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunli","family":"Liu","sequence":"additional","affiliation":[{"name":"School of Biotechnology and Key Laboratory of Industrial Biotechnology of Ministry of Education, Jiangnan University, Wuxi 214122, China"},{"name":"National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi 214122, China"},{"name":"Jiangsu Provincial Engineering Research Center for Bioactive Product Processing, Jiangnan University, Wuxi 214122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ye","family":"Li","sequence":"additional","affiliation":[{"name":"School of Biotechnology and Key Laboratory of Industrial Biotechnology of Ministry of Education, Jiangnan University, Wuxi 214122, China"},{"name":"National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi 214122, China"},{"name":"Jiangsu Provincial Engineering Research Center for Bioactive Product Processing, Jiangnan University, Wuxi 214122, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhonghu","family":"Bai","sequence":"additional","affiliation":[{"name":"School of Biotechnology and Key Laboratory of Industrial Biotechnology of Ministry of Education, Jiangnan University, Wuxi 214122, China"},{"name":"National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, Jiangnan University, Wuxi 214122, China"},{"name":"Jiangsu Provincial Engineering Research Center for Bioactive Product Processing, Jiangnan University, Wuxi 214122, China"},{"name":"Zhengzhou University of Technology, Zhengzhou 450044, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,5,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"79981","DOI":"10.7554\/eLife.79981","article-title":"Phage resistance profiling identifies new genes required for biogenesis and modification of the corynebacterial cell envelope","volume":"11","author":"McKitterick","year":"2017","journal-title":"eLife"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1038\/s41589-018-0206-1","article-title":"Sequential assembly of the septal cell envelope prior to V snapping in Corynebacterium glutamicum","volume":"15","author":"Zhou","year":"2019","journal-title":"Nat. Chem. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Lim, H.C., Sher, J.W., Rodriguez-Rivera, F.P., Fumeaux, C., Bertozzi, C.R., and Bernhardt, T.G. (2019). Identification of new components of the RipC-FtsEX cell separation pathway of Corynebacterineae. PLoS Genet., 15.","DOI":"10.1371\/journal.pgen.1008284"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1038\/s41579-018-0055-7","article-title":"Structural insights into the signalling mechanisms of two-component systems","volume":"16","author":"Mechaly","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Wu, X., Liu, J., Liu, Z., Gong, G., and Zha, J. (2022). Microbial cell surface engineering for high-level synthesis of bio-products. Biotechnol. Adv., 55.","DOI":"10.1016\/j.biotechadv.2022.107912"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Qin, X., Zhang, K., Nie, Y., and Wu, X.L. (2022). The roles of the two-component system, MtrAB, in response to diverse cell envelope stresses in Dietzia sp. DQ12-45-1b. Appl. Environ. Microbiol., 88.","DOI":"10.1128\/aem.01337-22"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Mike, L.A., Choby, J.E., Brinkman, P.R., Olive, L.Q., Dutter, B.F., Ivan, S.J., Gibbs, C.M., Sulikowski, G.A., Stauff, D.L., and Skaar, E.P. (2014). Two-component system cross-regulation integrates Bacillus anthracis response to heme and cell envelope stress. PLoS Pathog., 10.","DOI":"10.1371\/journal.ppat.1004044"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e0039022","DOI":"10.1128\/jb.00390-22","article-title":"A copper-responsive two-component system governs lipoprotein remodeling in Listeria monocytogenes","volume":"205","author":"Komazin","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/j.cell.2009.08.032","article-title":"Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction","volume":"139","author":"Casino","year":"2009","journal-title":"Cell"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Trajtenberg, F., Albanesi, D., Ru\u00e9talo, N., Botti, H., Mechaly, A.E., Nieves, M., Aguilar, P.S., Cybulski, L., Larrieux, N., and de Mendoza, D. (2014). Allosteric activation of bacterial response regulators: The role of the cognate histidine kinase beyond phosphorylation. mBio, 5.","DOI":"10.1128\/mBio.02105-14"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1038\/s41589-019-0286-6","article-title":"Rewiring bacterial two-component systems by modular DNA-binding domain swapping","volume":"15","author":"Schmidl","year":"2019","journal-title":"Nat. Chem. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"MGM2-0010-2013","DOI":"10.1128\/microbiolspec.MGM2-0010-2013","article-title":"Two-component regulatory systems of Mycobacteria","volume":"2","author":"Parish","year":"2014","journal-title":"Microbiol. Spectr."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1111\/j.1365-2958.2004.04249.x","article-title":"Deletion of the genes encoding the MtrA-MtrB two-component system of Corynebacterium glutamicum has a strong influence on cell morphology, antibiotics susceptibility and expression of genes involved in osmoprotection","volume":"54","author":"Brocker","year":"2004","journal-title":"Mol. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2134","DOI":"10.1128\/JB.188.6.2134-2143.2006","article-title":"MprAB is a stress-responsive two-component system that directly regulates expression of sigma factors SigB and SigE in Mycobacterium tuberculosis","volume":"188","author":"He","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1111\/j.1365-2958.2007.05814.x","article-title":"Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria","volume":"65","author":"Sureka","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"12706","DOI":"10.1073\/pnas.221272198","article-title":"Mycobacterium tuberculosis signal transduction system required for persistent infections","volume":"98","author":"Zahrt","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1111\/mmi.13037","article-title":"The Psp system of Mycobacterium tuberculosis integrates envelope stress-sensing and envelope-preserving functions","volume":"97","author":"Datta","year":"2015","journal-title":"Mol. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"5105","DOI":"10.1128\/JB.05562-11","article-title":"Components of the Rv0081-Rv0088 locus, which encodes a predicted formate hydrogenlyase complex, are coregulated by Rv0081, MprA, and DosR in Mycobacterium tuberculosis","volume":"193","author":"He","year":"2011","journal-title":"J. Bacteriol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"3018","DOI":"10.1128\/IAI.00520-12","article-title":"MprA and DosR coregulate a Mycobacterium tuberculosis virulence operon encoding Rv1813c and Rv1812c","volume":"80","author":"Bretl","year":"2012","journal-title":"Infect. Immun."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"6213","DOI":"10.1128\/JB.00492-07","article-title":"Regulation of the alpha-crystallin gene acr2 by the MprAB two-component system of Mycobacterium tuberculosis","volume":"189","author":"Pang","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1128\/JB.01067-12","article-title":"MprAB regulates the espA operon in Mycobacterium tuberculosis and modulates ESX-1 function and host cytokine response","volume":"195","author":"Pang","year":"2013","journal-title":"J. Bacteriol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1128\/JB.187.1.202-212.2005","article-title":"Identification and characterization of a regulatory sequence recognized by Mycobacterium tuberculosis persistence regulator MprA","volume":"187","author":"He","year":"2005","journal-title":"J. Bacteriol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Sureka, K., Ghosh, B., Dasgupta, A., Basu, J., Kundu, M., and Bose, I. (2008). Positive feedback and noise activate the stringent response regulator rel in mycobacteria. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0001771"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.tube.2011.10.024","article-title":"The \u03b2-propeller gene Rv1057 of Mycobacterium tuberculosis has a complex promoter directly regulated by both the MprAB and TrcRS two-component systems","volume":"91","author":"Pang","year":"2011","journal-title":"Tuberculosis"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1099\/mic.0.29281-0","article-title":"Evidence for complex interactions of stress-associated regulons in an mprAB deletion mutant of Mycobacterium tuberculosis","volume":"153","author":"Pang","year":"2007","journal-title":"Microbiology"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1128\/JB.01064-13","article-title":"The MprB extracytoplasmic domain negatively regulates activation of the Mycobacterium tuberculosis MprAB two-component system","volume":"196","author":"Bretl","year":"2014","journal-title":"J. Bacteriol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Wong, K.W. (2017). The Role of ESX-1 in Mycobacterium tuberculosis Pathogenesis. Microbiol. Spectr., 5.","DOI":"10.1128\/microbiolspec.TBTB2-0001-2015"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"6962","DOI":"10.1128\/IAI.71.12.6962-6970.2003","article-title":"Functional analysis of the Mycobacterium tuberculosis MprAB two-component signal transduction system","volume":"71","author":"Zahrt","year":"2003","journal-title":"Infect. Immun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1781","DOI":"10.1007\/s10295-019-02240-z","article-title":"Understanding high \u03b5-poly-L-lysine production by Streptomyces albulus using pH shock strategy in the level of transcriptomic","volume":"46","author":"Pan","year":"2019","journal-title":"J. Ind. Microbiol. Biotechnol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1007\/s00253-015-7074-3","article-title":"Regulons of global transcription factors in Corynebacterium glutamicum","volume":"100","author":"Toyoda","year":"2016","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1111\/mmi.13839","article-title":"The three-component system EsrISR regulates a cell envelope stress response in Corynebacterium glutamicum","volume":"106","author":"Kleine","year":"2017","journal-title":"Mol. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5595","DOI":"10.1128\/jb.175.17.5595-5603.1993","article-title":"Isoleucine synthesis in Corynebacterium glutamicum: Molecular analysis of the ilvB-ilvN-ilvC operon","volume":"175","author":"Keilhauer","year":"1993","journal-title":"J. Bacteriol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Gao, G.R., Wei, S.Y., Ding, M.Z., Hou, Z.J., Wang, D.J., Xu, Q.M., and Chen, Y.J. (2003). Enhancing fengycin production in the co-culture of Bacillus subtilis and Corynebacterium glutamicum by engineering proline transporter. Bioresour. Technol., 383.","DOI":"10.1016\/j.biortech.2023.129229"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"SEQC\/MAQC-III Consortium (2014). A comprehensive assessment of RNA-seq accuracy, reproducibility and information content by the Sequencing Quality Control Consortium. Nat. Biotechnol., 32, 903\u2013914.","DOI":"10.1038\/nbt.2957"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1038\/s41598-017-01617-3","article-title":"Benchmarking of RNA-sequencing analysis workflows using whole-transcriptome RT-qPCR expression data","volume":"7","author":"Everaert","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3045","DOI":"10.1128\/JB.00406-16","article-title":"Impact of LytR-CpsA-Psr proteins on cell wall biosynthesis in Corynebacterium glutamicum","volume":"198","author":"Baumgart","year":"2016","journal-title":"J. Bacteriol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1111\/mmi.13883","article-title":"Extracytoplasmic function sigma factor \u03c3D confers resistance to environmental stress by enhancing mycolate synthesis and modifying peptidoglycan structures in Corynebacterium glutamicum","volume":"107","author":"Toyoda","year":"2018","journal-title":"Mol. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/mmi.14492","article-title":"The C-terminal domain of Corynebacterium glutamicum mycoloyltransferase A is composed of five repeated motifs involved in cell wall binding and stability","volume":"114","author":"Dietrich","year":"2020","journal-title":"Mol. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s00203-003-0556-1","article-title":"Identification and functional analysis of six mycolyltransferase genes of Corynebacterium glutamicum ATCC 13032: The genes cop1, cmt1, and cmt2 can replace each other in the synthesis of trehalose dicorynomycolate, a component of the mycolic acid layer of the cell envelope","volume":"180","author":"Brand","year":"2003","journal-title":"Arch. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"4385","DOI":"10.1111\/febs.12028","article-title":"Corynebacterium glutamicum Zur acts as a zinc-sensing transcriptional repressor of both zinc-inducible and zinc-repressible genes involved in zinc homeostasis","volume":"279","author":"Teramoto","year":"2012","journal-title":"FEBS J."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1186\/1471-2164-14-888","article-title":"Comprehensive analysis of the Corynebacterium glutamicum transcriptome using an improved RNAseq technique","volume":"14","author":"Mentz","year":"2013","journal-title":"BMC Genom."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Schr\u00f6der, J., Jochmann, N., Rodionov, D.A., and Tauch, A. (2010). The Zur regulon of Corynebacterium glutamicum ATCC 13032. BMC Genom., 7.","DOI":"10.1186\/1471-2164-11-12"},{"key":"ref_43","first-page":"51","article-title":"Comparative Analysis of the Bacterial Membrane Disruption Effect of Two Natural Plant Antimicrobial Peptides","volume":"23","author":"Farkas","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Li, H., Xu, D., Tan, X., Huang, D., Huang, Y., Zhao, G., Hu, X., and Wang, X. (2023). The role of trehalose biosynthesis on mycolate composition and L-glutamate production in Corynebacterium glutamicum. Microbiol. Res., 267.","DOI":"10.1016\/j.micres.2022.127260"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"7639","DOI":"10.1128\/JB.187.22.7639-7646.2005","article-title":"Functional analysis of all aminotransferase proteins inferred from the genome sequence of Corynebacterium glutamicum","volume":"187","author":"Marienhagen","year":"2005","journal-title":"J. Bacteriol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"7112","DOI":"10.1128\/JB.186.21.7112-7122.2004","article-title":"Classification and strength measurement of stationary-phase promoters by use of a newly developed promoter cloning vector","volume":"186","author":"Shimada","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1186\/s12934-019-1273-z","article-title":"A secretion biosensor for monitoring Sec-dependent protein export in Corynebacterium glutamicum","volume":"19","author":"Jurischka","year":"2020","journal-title":"Microb. Cell Fact."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"750150","DOI":"10.3389\/fmicb.2021.750150","article-title":"Biosensor-Based Optimization of Cutinase Secretion by Corynebacterium glutamicum","volume":"12","author":"Bakkes","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1128\/JB.01167-09","article-title":"PepD participates in the mycobacterial stress response mediated through MprAB and SigE","volume":"192","author":"White","year":"2010","journal-title":"J. Bacteriol."}],"updated-by":[{"DOI":"10.3390\/microorganisms14071576","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2025,5,13]],"date-time":"2025-05-13T00:00:00Z","timestamp":1747094400000}}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/5\/1120\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T06:24:14Z","timestamp":1784528654000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/13\/5\/1120"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5,13]]},"references-count":49,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,5]]}},"alternative-id":["microorganisms13051120"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms13051120","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,5,13]]}}}