{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,15]],"date-time":"2026-09-15T22:48:16Z","timestamp":1789512496913,"version":"build-2803163510"},"reference-count":64,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2021,11,6]],"date-time":"2021-11-06T00:00:00Z","timestamp":1636156800000},"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 malaria parasite Plasmodium\u00a0falciparum undergoes closed mitosis, which occurs within an intact nuclear envelope, and differs significantly from its human host. Mitosis is underpinned by the dynamics of microtubules and the nuclear envelope. To date, our ability to study P. falciparum mitosis by microscopy has been hindered by the small size of the P. falciparum nuclei. Ultrastructure expansion microscopy (U-ExM) has recently been developed for P. falciparum, allowing the visualization of mitosis at the individual nucleus level. Using U-ExM, three intranuclear microtubule structures are observed: hemispindles, mitotic spindles, and interpolar spindles. A previous study demonstrated that the mini-chromosome maintenance complex binding-protein (MCMBP) depletion caused abnormal nuclear morphology and microtubule defects. To investigate the role of microtubules following MCMBP depletion and study the nuclear envelope in these parasites, we developed the first nuclear stain enabled by U-ExM in P. falciparum. MCMBP-deficient parasites show aberrant hemispindles and mitotic spindles. Moreover, anaphase chromatin bridges and individual nuclei containing multiple microtubule structures were observed following MCMBP knockdown. Collectively, this study refines our understanding of MCMBP-deficient parasites and highlights the utility of U-ExM coupled with a nuclear envelope stain for studying mitosis in P. falciparum.<\/jats:p>","DOI":"10.3390\/microorganisms9112306","type":"journal-article","created":{"date-parts":[[2021,11,7]],"date-time":"2021-11-07T20:41:14Z","timestamp":1636317674000},"page":"2306","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":91,"title":["Expansion Microscopy Reveals Plasmodium falciparum Blood-Stage Parasites Undergo Anaphase with A Chromatin Bridge in the Absence of Mini-Chromosome Maintenance Complex Binding Protein"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1573-6139","authenticated-orcid":false,"given":"Benjamin","family":"Liffner","sequence":"first","affiliation":[{"name":"Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN 46202, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2468-8156","authenticated-orcid":false,"given":"Sabrina","family":"Absalon","sequence":"additional","affiliation":[{"name":"Department of Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN 46202, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,11,6]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (2020). World Malaria Report 2020, WHO."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1470","DOI":"10.1016\/S1473-3099(20)30228-0","article-title":"Molecular epidemiology of resistance to antimalarial drugs in the Greater Mekong subregion: An observational study","volume":"20","author":"Imwong","year":"2020","journal-title":"Lancet Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"a025619","DOI":"10.1101\/cshperspect.a025619","article-title":"Antimalarial Drug Resistance: A Threat to Malaria Elimination","volume":"7","author":"Menard","year":"2017","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1056\/NEJMoa1314981","article-title":"Spread of Artemisinin Resistance in Plasmodium falciparum Malaria","volume":"371","author":"Ashley","year":"2014","journal-title":"N. Engl. J. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1602","DOI":"10.1038\/s41591-020-1005-2","article-title":"Emergence and clonal expansion of in vitro artemisinin-resistant Plasmodium falciparum kelch13 R561H mutant parasites in Rwanda","volume":"26","author":"Uwimana","year":"2020","journal-title":"Nat. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1056\/NEJMoa2101746","article-title":"Evidence of Artemisinin-Resistant Malaria in Africa","volume":"385","author":"Balikagala","year":"2021","journal-title":"N. Engl. J. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1719","DOI":"10.1039\/C9MD00120D","article-title":"Quinolone antibiotics","volume":"10","author":"Pham","year":"2019","journal-title":"MedChemComm"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1007\/s00253-004-1783-3","article-title":"Inhibitors of virus replication: Recent developments and prospects","volume":"66","author":"Magden","year":"2004","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"78","DOI":"10.3389\/fmolb.2017.00078","article-title":"Inhibiting DNA Polymerases as a Therapeutic Intervention against Cancer","volume":"4","author":"Berdis","year":"2017","journal-title":"Front. Mol. Biosci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"3875","DOI":"10.2147\/DDDT.S265602","article-title":"Recent Progress in the Development of New Antimalarial Drugs with Novel Targets","volume":"ume 14","author":"Belete","year":"2020","journal-title":"Drug Des. Dev. Ther."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1038\/nrmicro3184","article-title":"Cell division in apicomplexan parasites","volume":"12","author":"Francia","year":"2014","journal-title":"Nat. Rev. Genet."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Rudlaff, R.M., Kraemer, S., Marshman, J., and Dvorin, J.D. (2020). Three-dimensional ultrastructure of Plasmodium falciparum throughout cytokinesis. PLoS Pathog., 16.","DOI":"10.1371\/journal.ppat.1008587"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2181","DOI":"10.1038\/s41467-019-10214-z","article-title":"An essential contractile ring protein controls cell division in Plasmodium falciparum","volume":"10","author":"Rudlaff","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1128\/EC.00314-10","article-title":"Mitosis in the Human Malaria Parasite Plasmodium falciparum","volume":"10","author":"Gerald","year":"2011","journal-title":"Eukaryot. Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1017\/S0031182000075041","article-title":"Microtubular organization visualized by immunofluorescence microscopy during erythrocytic schizogony in Plasmodium falciparumand investigation of post-translational modifications of parasite tubulin","volume":"106","author":"Read","year":"1993","journal-title":"Parasitology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e202101199","DOI":"10.26508\/lsa.202101199","article-title":"An extended DNA-free intranuclear compartment organizes centrosome microtubules in malaria parasites","volume":"4","author":"Simon","year":"2021","journal-title":"Life Sci. Alliance"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.molbiopara.2019.02.007","article-title":"Immunofluorescence staining protocol for STED nanoscopy of Plasmodium-infected red blood cells","volume":"229","author":"Mehnert","year":"2019","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1016\/S0022-5320(77)90043-0","article-title":"Etude ultrastructurale des mitoses multiples au cours de la sporogonie du Plasmodium b. berghei","volume":"59","author":"Bafort","year":"1977","journal-title":"J. Ultrastruct. Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.molbiopara.2005.08.020","article-title":"Cellular and molecular actions of dinitroaniline and phosphorothioamidate herbicides on Plasmodium falciparum: Tubulin as a specific antimalarial target","volume":"145","author":"Fennell","year":"2006","journal-title":"Mol. Biochem. Parasitol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/j.ijpara.2007.09.005","article-title":"Isotype expression, post-translational modification and stage-dependent production of tubulins in erythrocytic Plasmodium falciparum","volume":"38","author":"Fennell","year":"2008","journal-title":"Int. J. Parasitol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Zeeshan, M., Pandey, R., Ferguson, D., Tromer, E.C., Markus, R., Abel, S., Brady, D., Daniel, E., Limenitakis, R., and Bottrill, A.R. (2020). Real-time dynamics of Plasmodium NDC80 reveals unusual modes of chromosome segregation during parasite proliferation. J. Cell Sci., 134.","DOI":"10.1242\/jcs.245753"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Bertiaux, E., Balestra, A.C., Bournonville, L., Louvel, V., Maco, B., Soldati-Favre, D., Brochet, M., Guichard, P., and Hamel, V. (2021). Expansion microscopy provides new insights into the cytoskeleton of malaria parasites including the conservation of a conoid. PLoS Biol., 19.","DOI":"10.1371\/journal.pbio.3001401"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Rashpa, R., and Brochet, M. (2021). Ultrastructure expansion microscopy of Plasmodium gametocytes reveals the molecular architecture of a microtubule organisation centre coordinating mitosis with axoneme assembly. bioRxiv, 453039.","DOI":"10.1101\/2021.07.21.453039"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1038\/s41586-020-2648-3","article-title":"Closed mitosis requires local disassembly of the nuclear envelope","volume":"585","author":"Dey","year":"2020","journal-title":"Nature"},{"key":"ref_25","first-page":"e13284","article-title":"Depletion of the mini-chromosome maintenance complex binding protein allows the progression of cytokinesis despite abnormal karyokinesis during the asexual development of Plasmodium falciparum","volume":"23","author":"Absalon","year":"2020","journal-title":"Cell. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1016\/j.neo.2014.07.011","article-title":"Deregulation of the Replisome Factor MCMBP Prompts Oncogenesis in Colorectal Carcinomas through Chromosomal Instability","volume":"16","author":"Quimbaya","year":"2014","journal-title":"Neoplasia"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1242\/jcs.089938","article-title":"The MCM-associated protein MCM-BP is important for human nuclear morphology","volume":"125","author":"Jagannathan","year":"2012","journal-title":"J. Cell Sci."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Kim, H.-S., Park, S.H., G\u00fcnzl, A., and Cross, G.A.M. (2013). MCM-BP Is Required for Repression of Life-Cycle Specific Genes Transcribed by RNA Polymerase I in the Mammalian Infectious Form of Trypanosoma brucei. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0057001"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-018-2800-1","article-title":"Checks and balances? DNA replication and the cell cycle in Plasmodium","volume":"11","author":"Matthews","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1126\/science.781840","article-title":"Human Malaria Parasites in Continuous Culture","volume":"193","author":"Trager","year":"1976","journal-title":"Science"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1038\/nmeth1132","article-title":"An FKBP destabilization domain modulates protein levels in Plasmodium falciparum","volume":"4","author":"Armstrong","year":"2007","journal-title":"Nat. Methods"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1186\/1475-2875-3-7","article-title":"One-step concentration of malarial parasite-infected red blood cells and removal of contaminating white blood cells","volume":"3","author":"Trang","year":"2004","journal-title":"Malar. J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"418","DOI":"10.2307\/3280287","article-title":"Synchronization of Plasmodium falciparum Erythrocytic Stages in Culture","volume":"65","author":"Lambros","year":"1979","journal-title":"J. Parasitol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1186\/1475-2875-7-45","article-title":"Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species","volume":"7","author":"Ribaut","year":"2008","journal-title":"Malar. J."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1073\/pnas.98.1.271","article-title":"Malaria parasite exit from the host erythrocyte: A two-step process requiring extraerythrocytic proteolysis","volume":"98","author":"Salmon","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/bs.mcb.2020.05.006","article-title":"Ultrastructure expansion microscopy (U-ExM)","volume":"161","author":"Gambarotto","year":"2020","journal-title":"Methods Cell Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1457","DOI":"10.1111\/cmi.12132","article-title":"Electron tomography of Plasmodium falciparum merozoites reveals core cellular events that underpin erythrocyte invasion","volume":"15","author":"Hanssen","year":"2013","journal-title":"Cell. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"3825","DOI":"10.1242\/jcs.00665","article-title":"Plasmodium falciparum apical membrane antigen 1 (PfAMA-1) is translocated within micronemes along subpellicular microtubules during merozoite development","volume":"116","author":"Bannister","year":"2003","journal-title":"J. Cell Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1128\/EC.00023-13","article-title":"Nuclear Pores and Perinuclear Expression Sites of var and Ribosomal DNA Genes Correspond to Physically Distinct Regions in Plasmodium falciparum","volume":"12","author":"Guizetti","year":"2013","journal-title":"Eukaryot. Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"11249","DOI":"10.1038\/s41598-018-29590-5","article-title":"Nuclear Pore Complex Components in the Malaria Parasite Plasmodium berghei","volume":"8","author":"Kehrer","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_41","first-page":"2053","article-title":"Origin, composition, organization and function of the inner membrane complex of Plasmodium falciparum gametocytes","volume":"125","author":"Dearnley","year":"2012","journal-title":"J. Cell Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/ncomms1169","article-title":"Development and host cell modifications of Plasmodium falciparum blood stages in four dimensions","volume":"2","author":"Heiber","year":"2011","journal-title":"Nat. Commun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2856","DOI":"10.1016\/j.bbamcr.2015.08.007","article-title":"Eps15 homology domain containing protein of Plasmodium falciparum (PfEHD) associates with endocytosis and vesicular trafficking towards neutral lipid storage site","volume":"1853","author":"Thakur","year":"2015","journal-title":"Biochim. Biophys. Acta Bioenergy"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"4773","DOI":"10.1038\/ncomms5773","article-title":"A female gametocyte-specific ABC transporter plays a role in lipid metabolism in the malaria parasite","volume":"5","author":"Tran","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1186\/s12936-016-1130-z","article-title":"Changes in lipid composition during sexual development of the malaria parasite Plasmodium falciparum","volume":"15","author":"Tran","year":"2016","journal-title":"Malar. J."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1128\/EC.00228-14","article-title":"Host Erythrocyte Environment Influences the Localization of Exported Protein 2, an Essential Component of the Plasmodium Translocon","volume":"14","author":"Meibalan","year":"2015","journal-title":"Eukaryot. Cell"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"6532","DOI":"10.1074\/jbc.M207039200","article-title":"The Signal Sequence of Exported Protein-1 Directs the Green Fluorescent Protein to the Parasitophorous Vacuole of Transfected Malaria Parasites","volume":"278","author":"Adisa","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Finardi, A., Massari, L.F., and Visintin, R. (2020). Anaphase Bridges: Not All Natural Fibers Are Healthy. Genes, 11.","DOI":"10.3390\/genes11080902"},{"key":"ref_49","unstructured":"Bradshaw, R.A., and Stahl, P.D. (2016). Regulating Cytokinesis. Encyclopedia of Cell Biology, Academic Press."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Koreny, L., Zeeshan, M., Barylyuk, K., Tromer, E.C., van Hooff, J.J.E., Brady, D., Ke, H., Chelaghma, S., Ferguson, D.J.P., and Eme, L. (2021). Molecular characterization of the conoid complex in Toxoplasma reveals its conservation in all apicomplexans, including Plasmodium species. PLoS Biol., 19.","DOI":"10.1371\/journal.pbio.3001081"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1017\/S0031182000064064","article-title":"Lamellar membranes associated with rhoptries in erythrocytic merozoites of Plasmodium knowlesi: A clue to the mechanism of invasion","volume":"92","author":"Bannister","year":"1986","journal-title":"Parasitology"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1016\/j.pt.2021.03.006","article-title":"The Ins and Outs of Plasmodium Rhoptries, Focusing on the Cytosolic Side","volume":"37","author":"Liffner","year":"2021","journal-title":"Trends Parasitol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"3044","DOI":"10.1128\/MCB.02384-06","article-title":"Identification and Characterization of a Novel Component of the Human Minichromosome Maintenance Complex","volume":"27","author":"Sakwe","year":"2007","journal-title":"Mol. Cell. Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1101\/gad.614411","article-title":"MCM-BP regulates unloading of the MCM2-7 helicase in late S phase","volume":"25","author":"Nishiyama","year":"2010","journal-title":"Genes Dev."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Takahashi, N., Quimbaya, M., Schubert, V., Lammens, T., Vandepoele, K., Schubert, I., Matsui, M., Inze, D., Berx, G., and De Veylder, L. (2010). The MCM-Binding Protein ETG1 Aids Sister Chromatid Cohesion Required for Postreplicative Homologous Recombination Repair. PLoS Genet., 6.","DOI":"10.1371\/journal.pgen.1000817"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"26238","DOI":"10.1074\/jbc.M302699200","article-title":"Biochemical Analysis of the Yeast Condensin Smc2\/4 Complex: An ATPase that promotes knotting of circular DNA","volume":"278","author":"Stray","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1111\/tpj.14639","article-title":"The condensin subunits SMC2 and SMC4 interact for correct condensation and segregation of mitotic maize chromosomes","volume":"102","author":"Wang","year":"2019","journal-title":"Plant J."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1883","DOI":"10.1016\/j.celrep.2020.01.033","article-title":"Plasmodium Condensin Core Subunits SMC2\/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission","volume":"30","author":"Pandey","year":"2020","journal-title":"Cell Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1101\/gad.9.5.587","article-title":"SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family","volume":"9","author":"Strunnikov","year":"1995","journal-title":"Genes Dev."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/S0960-9822(01)00096-3","article-title":"A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis","volume":"11","author":"Steffensen","year":"2001","journal-title":"Curr. Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"728","DOI":"10.1038\/s41467-018-03135-w","article-title":"LEM-3 is a midbody-tethered DNA nuclease that resolves chromatin bridges during late mitosis","volume":"9","author":"Hong","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"eaap7847","DOI":"10.1126\/science.aap7847","article-title":"Uncovering the essential genes of the human malaria parasite Plasmodium falciparum by saturation mutagenesis","volume":"360","author":"Zhang","year":"2018","journal-title":"Science"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1016\/j.cell.2017.06.030","article-title":"Functional Profiling of a Plasmodium Genome Reveals an Abundance of Essential Genes","volume":"170","author":"Bushell","year":"2017","journal-title":"Cell"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1017\/S0031182000046266","article-title":"The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei","volume":"67","author":"Canning","year":"1973","journal-title":"Parasitology"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/11\/2306\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:26:52Z","timestamp":1760167612000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/9\/11\/2306"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,11,6]]},"references-count":64,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["microorganisms9112306"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms9112306","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,11,6]]}}}