{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,25]],"date-time":"2026-09-25T16:02:20Z","timestamp":1790352140201,"version":"4.1.0"},"reference-count":86,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T00:00:00Z","timestamp":1788220800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Erasmus+ traineeship"},{"name":"Swedish Institute Scholarship for Global Professionals"},{"id":[{"id":"https:\/\/ror.org\/022w3f533","id-type":"ROR","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004359","name":"Swedish Research Council for Natural Sciences and Engineering","doi-asserted-by":"publisher","award":["2022-04865"],"award-info":[{"award-number":["2022-04865"]}],"id":[{"id":"10.13039\/501100004359","id-type":"DOI","asserted-by":"publisher"}]},{"award":["2022-04865"],"award-info":[{"award-number":["2022-04865"]}],"id":[{"id":"https:\/\/ror.org\/03zttf063","id-type":"ROR","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>The phosphoethanolamine-modified exopolysaccharide cellulose synthesized by the type IIa cellulose biosynthesis nanomachine is a major extracellular matrix component of Escherichia coli. Here, we aim to investigate whether homologs of bcsABC genes of the core genome EcType 1 bcs cellulose biosynthesis gene cluster, which are diminished or abolished in high-virulence isolates, and entire clusters are mobilized on plasmids and occasionally manifested on E. coli chromosomes at alternative locations. While EcType BcsA2 and BcsA3 cellulose synthases are restricted to the genus Escherichia, the EcType BcsA4 cellulose synthase and associated bcs gene products are highly similar to Klebsiella pneumoniae counterparts. Cyclic di-GMP turnover proteins not previously recognized to post-translationally regulate cellulose biosynthesis on the chromosomal level are frequently co-localized with novel bcs genes. Thermotolerant meat-derived E. coli 730V1 uniquely harbors an EcType 4 bcs gene cluster of type Ib with a type IIb bcsG gene on a plasmid. Chemical, phenotypic and genetic evidence showed cellulose biosynthesis, cellulose-dependent cell aggregation and activation of biosynthesis by the second messenger cyclic di-GMP, an allosteric activator of the cellulose synthase. With gene duplication, horizontal gene transfer and recombination to contribute to the multiplication and diversification of bcs gene clusters in a number of different bacterial species, the extent and ecological role(s) of the multiplication, transfer and replacement of cellulose biosynthesis gene clusters, as well as in species other than E. coli, still need to be unraveled. Our data indicate, however, that although diversification and multiplication of bcs clusters is ongoing in the species E. coli, these events become rarely manifested in the population.<\/jats:p>","DOI":"10.3390\/microorganisms14091932","type":"journal-article","created":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T11:33:32Z","timestamp":1788262412000},"page":"1932","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":1,"title":["Diverse Horizontally Transferred Cellulose Biosynthesis Gene Clusters in Escherichia coli Strains"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0009-0008-7123-9664","authenticated-orcid":false,"given":"Seyedmohammad","family":"Hosseinpourlamardi","sequence":"first","affiliation":[{"name":"Department of Microbiology, Tumor and Cell Biology, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"given":"Shaiqa","family":"Labiba","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tumor and Cell Biology, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-7885-8108","authenticated-orcid":false,"given":"Li","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tumor and Cell Biology, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-0938-5125","authenticated-orcid":false,"given":"Ali","family":"Dadvar","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tumor and Cell Biology, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5266-1746","authenticated-orcid":false,"given":"Manita","family":"Guragain","sequence":"additional","affiliation":[{"name":"Characterization and Interventions for Foodborne Pathogens, Agricultural Research Service, United States Department of Agriculture, Wyndmoor, PA 19038, USA"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3812-6621","authenticated-orcid":false,"given":"Ute","family":"R\u00f6mling","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tumor and Cell Biology, Biomedicum, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"writing-original-draft","vocabulary":"credit"},{"role":"project-administration","vocabulary":"credit"},{"role":"funding-acquisition","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3358","DOI":"10.1002\/anie.200460587","article-title":"Cellulose: Fascinating biopolymer and sustainable raw material","volume":"44","author":"Klemm","year":"2005","journal-title":"Angew. Chem. Int. Ed. Engl."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1016\/j.fgb.2009.07.001","article-title":"Identification of the cellulose synthase genes from the Oomycete Saprolegnia monoica and effect of cellulose synthesis inhibitors on gene expression and enzyme activity","volume":"46","author":"Fugelstad","year":"2009","journal-title":"Fungal Genet. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s00427-003-0379-8","article-title":"The evolutionary origin of animal cellulose synthase","volume":"214","author":"Nakashima","year":"2004","journal-title":"Dev. Genes. Evol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/j.molp.2022.12.015","article-title":"Cellulose synthesis in land plants","volume":"16","author":"Pedersen","year":"2023","journal-title":"Mol. Plant"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1016\/j.tim.2015.05.005","article-title":"Bacterial cellulose biosynthesis: Diversity of operons, subunits, products, and functions","volume":"23","author":"Galperin","year":"2015","journal-title":"Trends Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Scott, W., Lowrance, B., Anderson, A.C., and Weadge, J.T. (2020). Identification of the Clostridial cellulose synthase and characterization of the cognate glycosyl hydrolase, CcsZ. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0242686"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1186\/s12934-016-0576-6","article-title":"BcsZ inhibits biofilm phenotypes and promotes virulence by blocking cellulose production in Salmonella enterica serovar Typhimurium","volume":"15","author":"Ahmad","year":"2016","journal-title":"Microb. Cell Fact."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"7798","DOI":"10.1038\/s41467-024-51838-0","article-title":"Insights into phosphoethanolamine cellulose synthesis and secretion across the Gram-negative cell envelope","volume":"15","author":"Verma","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1186\/1475-2859-11-125","article-title":"Role of Rhizobium endoglucanase CelC2 in cellulose biosynthesis and biofilm formation on plant roots and abiotic surfaces","volume":"11","author":"Robledo","year":"2012","journal-title":"Microb. Cell Fact."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"13907","DOI":"10.1038\/s41598-019-50337-3","article-title":"Legumes display common and host-specific responses to the rhizobial cellulase CelC2 during primary symbiotic infection","volume":"9","author":"Menendez","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1126\/science.aao4096","article-title":"Phosphoethanolamine cellulose: A naturally produced chemically modified cellulose","volume":"359","author":"Thongsomboon","year":"2018","journal-title":"Science"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1046\/j.1365-2958.2003.03670.x","article-title":"Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose","volume":"50","author":"Spiers","year":"2003","journal-title":"Mol. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3170","DOI":"10.1016\/j.jmb.2018.07.008","article-title":"Structural and Functional Characterization of the BcsG Subunit of the Cellulose Synthase in Salmonella typhimurium","volume":"430","author":"Sun","year":"2018","journal-title":"J. Mol. Biol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2672","DOI":"10.1021\/acsinfecdis.0c00314","article-title":"A Cyclic di-GMP Network Is Present in Gram-Positive Streptococcus and Gram-Negative Proteus Species","volume":"6","author":"Liu","year":"2020","journal-title":"ACS Infect. Dis."},{"key":"ref_15","first-page":"E757","article-title":"Novel mixed-linkage beta-glucan activated by c-di-GMP in Sinorhizobium meliloti","volume":"112","author":"Lloret","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4526","DOI":"10.1038\/s41467-023-40214-z","article-title":"The Gram-positive bacterium Romboutsia ilealis harbors a polysaccharide synthase that can produce (1,3;1,4)-beta-D-glucans","volume":"14","author":"Chang","year":"2023","journal-title":"Nat. Commun."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1452","DOI":"10.1046\/j.1365-2958.2001.02337.x","article-title":"The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix","volume":"39","author":"Zogaj","year":"2001","journal-title":"Mol. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1171","DOI":"10.1099\/jmm.0.46064-0","article-title":"Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract","volume":"54","author":"Bokranz","year":"2005","journal-title":"J. Med. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5183","DOI":"10.1073\/pnas.1500989112","article-title":"Salmonella promotes virulence by repressing cellulose production","volume":"112","author":"Pontes","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1046\/j.1365-2958.2000.01822.x","article-title":"AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways","volume":"36","author":"Rohde","year":"2000","journal-title":"Mol. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1038\/s41467-024-45176-4","article-title":"A convergent evolutionary pathway attenuating cellulose production drives enhanced virulence of some bacteria","volume":"15","author":"Nhu","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e02265","DOI":"10.1128\/mBio.02265-15","article-title":"Loss of Multicellular Behavior in Epidemic African Nontyphoidal Salmonella enterica Serovar Typhimurium ST313 Strain D23580","volume":"7","author":"Singletary","year":"2016","journal-title":"mBio"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3780","DOI":"10.1128\/IAI.68.6.3780-3783.2000","article-title":"Curli loci of Shigella spp","volume":"68","author":"Sakellaris","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1128\/mSphere.00751-19","article-title":"Shigella flexneri Adherence Factor Expression in In Vivo-Like Conditions","volume":"4","author":"Chanin","year":"2019","journal-title":"mSphere"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5276","DOI":"10.1128\/jb.177.18.5276-5283.1995","article-title":"Identification of a second cellulose synthase gene (acsAII) in Acetobacter xylinum","volume":"177","author":"Saxena","year":"1995","journal-title":"J. Bacteriol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e02343-20","DOI":"10.1128\/AEM.02343-20","article-title":"Locus of Heat Resistance (LHR) in Meat-Borne Escherichia coli: Screening and Genetic Characterization","volume":"87","author":"Guragain","year":"2021","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1046\/j.1365-2958.1998.00791.x","article-title":"Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter","volume":"28","author":"Sierralta","year":"1998","journal-title":"Mol. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1123","DOI":"10.1111\/j.1365-2958.2004.04206.x","article-title":"GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility","volume":"53","author":"Simm","year":"2004","journal-title":"Mol. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"6640","DOI":"10.1073\/pnas.120163297","article-title":"One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products","volume":"97","author":"Datsenko","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/0378-1119(88)90330-7","article-title":"CLUSTAL: A package for performing multiple sequence alignment on a microcomputer","volume":"73","author":"Higgins","year":"1988","journal-title":"Gene"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-0716-1036-7_1","article-title":"The Clustal Omega Multiple Alignment Package","volume":"2231","author":"Sievers","year":"2021","journal-title":"Methods Mol. Biol."},{"key":"ref_33","first-page":"14","article-title":"GeneDoc: Analysis and Visualization of Genetic Variation","volume":"4","author":"Nicholas","year":"1997","journal-title":"EMBnet.news"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1102, 1104","DOI":"10.2144\/00286ir01","article-title":"The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences","volume":"28","author":"Stothard","year":"2000","journal-title":"Biotechniques"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"W320","DOI":"10.1093\/nar\/gku316","article-title":"Deciphering key features in protein structures with the new ENDscript server","volume":"42","author":"Robert","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3022","DOI":"10.1093\/molbev\/msab120","article-title":"MEGA11: Molecular Evolutionary Genetics Analysis Version 11","volume":"38","author":"Tamura","year":"2021","journal-title":"Mol. Biol. Evol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1093\/molbev\/msaa015","article-title":"IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era","volume":"37","author":"Minh","year":"2020","journal-title":"Mol. Biol. Evol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e0239821","DOI":"10.1128\/aem.02398-21","article-title":"Deciphering Molecular Mechanism Underlying Self-Flocculation of Zymomonas mobilis for Robust Production","volume":"88","author":"Cao","year":"2022","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1093\/bioinformatics\/btr039","article-title":"Easyfig: A genome comparison visualizer","volume":"27","author":"Sullivan","year":"2011","journal-title":"Bioinformatics"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1093\/bioinformatics\/17.7.646","article-title":"Evaluation of methods for the prediction of membrane spanning regions","volume":"17","author":"Moller","year":"2001","journal-title":"Bioinformatics"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"W401","DOI":"10.1093\/nar\/gkv485","article-title":"The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides","volume":"43","author":"Tsirigos","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S0923-2508(02)01316-5","article-title":"Molecular biology of cellulose production in bacteria","volume":"153","year":"2002","journal-title":"Res. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Oehme, D.P., Shafee, T., Downton, M.T., Bacic, A., and Doblin, M.S. (2019). Differences in protein structural regions that impact functional specificity in GT2 family beta-glucan synthases. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0224442"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"W420","DOI":"10.1093\/nar\/gkac373","article-title":"IBS 2.0: An upgraded illustrator for the visualization of biological sequences","volume":"50","author":"Xie","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1093\/bioinformatics\/btt607","article-title":"Protter: Interactive protein feature visualization and integration with experimental proteomic data","volume":"30","author":"Omasits","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1007\/978-1-4939-9877-7_20","article-title":"PlasmidFinder and In Silico pMLST: Identification and Typing of Plasmid Replicons in Whole-Genome Sequencing (WGS)","volume":"2075","author":"Carattoli","year":"2020","journal-title":"Methods Mol. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"D195","DOI":"10.1093\/nar\/gky1050","article-title":"PLSDB: A resource of complete bacterial plasmids","volume":"47","author":"Galata","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"W484","DOI":"10.1093\/nar\/gkad326","article-title":"Proksee: In-depth characterization and visualization of bacterial genomes","volume":"51","author":"Grant","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","article-title":"Prokka: Rapid prokaryotic genome annotation","volume":"30","author":"Seemann","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e00508","DOI":"10.1002\/mbo3.508","article-title":"Alterations of c-di-GMP turnover proteins modulate semi-constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli","volume":"6","author":"Cimdins","year":"2017","journal-title":"Microbiologyopen"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1046\/j.1462-2920.2001.00235.x","article-title":"Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium","volume":"3","author":"Gerstel","year":"2001","journal-title":"Environ. Microbiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1016\/S0003-2697(69)80009-6","article-title":"Semimicro determination of cellulose in biological materials","volume":"32","author":"Updegraff","year":"1969","journal-title":"Anal. Biochem."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/0009-8981(75)90119-9","article-title":"Oligosaccharides in urine of patients with glycoprotein storage diseases: I. Rapid detection by thin-layer chromatography","volume":"60","author":"Humbel","year":"1975","journal-title":"Clin. Chim. Acta"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1046\/j.1365-2958.2002.02802.x","article-title":"Genetic analysis of Salmonella enteritidis biofilm formation: Critical role of cellulose","volume":"43","author":"Solano","year":"2002","journal-title":"Mol. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1038\/nsmb.2803","article-title":"Mechanism of activation of bacterial cellulose synthase by cyclic di-GMP","volume":"21","author":"Morgan","year":"2014","journal-title":"Nat. Struct. Mol. Biol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2655","DOI":"10.1093\/nar\/gkab064","article-title":"Bacteria have numerous distinctive groups of phage-plasmids with conserved phage and variable plasmid gene repertoires","volume":"49","author":"Pfeifer","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1111\/mmi.14614","article-title":"A recently isolated human commensal Escherichia coli ST10 clone member mediates enhanced thermotolerance and tetrathionate respiration on a P1 phage-derived IncY plasmid","volume":"115","author":"Kamal","year":"2021","journal-title":"Mol. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1111\/mmi.12672","article-title":"GIL, a new c-di-GMP-binding protein domain involved in regulation of cellulose synthesis in enterobacteria","volume":"93","author":"Fang","year":"2014","journal-title":"Mol. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"8130","DOI":"10.1073\/pnas.87.20.8130","article-title":"Genetic organization of the cellulose synthase operon in Acetobacter xylinum","volume":"87","author":"Wong","year":"1990","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.cub.2023.11.057","article-title":"Structures and roles of BcsD and partner scaffold proteins in proteobacterial cellulose secretion","volume":"34","author":"Sana","year":"2024","journal-title":"Curr. Biol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"2513","DOI":"10.1007\/s00253-012-3948-9","article-title":"Genome-wide transcriptomic analysis of a flocculent strain of Zymomonas mobilis","volume":"93","author":"Jeon","year":"2012","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1038\/325279a0","article-title":"Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid","volume":"325","author":"Ross","year":"1987","journal-title":"Nature"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1038\/nrmicro2203","article-title":"Structural and mechanistic determinants of c-di-GMP signalling","volume":"7","author":"Schirmer","year":"2009","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_64","first-page":"e00790-16","article-title":"Progress in Understanding the Molecular Basis Underlying Functional Diversification of Cyclic Dinucleotide Turnover Proteins","volume":"199","author":"Liang","year":"2017","journal-title":"J. Bacteriol."},{"key":"ref_65","first-page":"001354","article-title":"Evolution of cyclic di-GMP signalling on a short and long term time scale","volume":"169","author":"Cao","year":"2023","journal-title":"Microbiology"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1128\/am.30.1.123-131.1975","article-title":"Production of cellulose microfibrils by Rhizobium","volume":"30","author":"Napoli","year":"1975","journal-title":"Appl. Microbiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"e00731","DOI":"10.1002\/mbo3.731","article-title":"Comparative genomics of the Komagataeibacter strains-Efficient bionanocellulose producers","volume":"8","author":"Ryngajllo","year":"2019","journal-title":"Microbiologyopen"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1159\/000519573","article-title":"Yin and Yang of Biofilm Formation and Cyclic di-GMP Signaling of the Gastrointestinal Pathogen Salmonella enterica Serovar Typhimurium","volume":"14","author":"Lamprokostopoulou","year":"2022","journal-title":"J. Innate Immun."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Kai-Larsen, Y., L\u00fcthje, P., Chromek, M., Peters, V., Wang, X., Holm, A., Kadas, L., Hedlund, K.O., Johansson, J., and Chapman, M.R. (2010). Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. PLoS Pathog., 6.","DOI":"10.1371\/journal.ppat.1001010"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Cimdins-Ahne, A., Naemi, A.O., Li, F., Simm, R., and R\u00f6mling, U. (2023). Characterisation of Variants of Cyclic di-GMP Turnover Proteins Associated with Semi-Constitutive rdar Morphotype Expression in Commensal and Uropathogenic Escherichia coli Strains. Microorganisms, 11.","DOI":"10.3390\/microorganisms11082048"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Bundalovic-Torma, C., Whitfield, G.B., Marmont, L.S., Howell, P.L., and Parkinson, J. (2020). A systematic pipeline for classifying bacterial operons reveals the evolutionary landscape of biofilm machineries. PLoS Comput. Biol., 16.","DOI":"10.1371\/journal.pcbi.1007721"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"2448","DOI":"10.1128\/aem.55.10.2448-2452.1989","article-title":"Alternative Environmental Roles for Cellulose Produced by Acetobacter xylinum","volume":"55","author":"Williams","year":"1989","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"8799","DOI":"10.1038\/s41467-024-53113-8","article-title":"Structural basis for synthase activation and cellulose modification in the E. coli Type II Bcs secretion system","volume":"15","author":"Anso","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"6123","DOI":"10.1038\/s41467-024-50331-y","article-title":"Characterization of a Salmonella enterica serovar Typhimurium lineage with rough colony morphology and multidrug resistance","volume":"15","author":"Xiang","year":"2024","journal-title":"Nat. Commun."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1146\/annurev.genet.38.072902.091600","article-title":"Mobile group II introns","volume":"38","author":"Lambowitz","year":"2004","journal-title":"Annu. Rev. Genet."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"3670","DOI":"10.1128\/JB.01920-07","article-title":"Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-D-glucosamine","volume":"190","author":"Itoh","year":"2008","journal-title":"J. Bacteriol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"3073","DOI":"10.1128\/JB.188.8.3073-3087.2006","article-title":"A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli","volume":"188","author":"Ghigo","year":"2006","journal-title":"J. Bacteriol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1111\/j.1462-2920.2008.01840.x","article-title":"Characterization of cellulose production in Escherichia coli Nissle 1917 and its biological consequences","volume":"11","author":"Monteiro","year":"2009","journal-title":"Environ. Microbiol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"113071","DOI":"10.1016\/j.jinorgbio.2025.113071","article-title":"Roles of biological heme-based sensors of O2 in controlling bacterial behavior","volume":"275","author":"Fekete","year":"2026","journal-title":"J. Inorg. Biochem."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1016\/j.jmb.2011.02.019","article-title":"Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing","volume":"407","author":"Tuckerman","year":"2011","journal-title":"J. Mol. Biol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"2901","DOI":"10.1099\/mic.0.041350-0","article-title":"The diguanylate cyclase YddV controls production of the exopolysaccharide poly-N-acetylglucosamine (PNAG) through regulation of the PNAG biosynthetic pgaABCD operon","volume":"156","author":"Tagliabue","year":"2010","journal-title":"Microbiology"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1111\/j.1574-695X.2010.00702.x","article-title":"The yddV-dos operon controls biofilm formation through the regulation of genes encoding curli fibers\u2019 subunits in aerobically growing Escherichia coli","volume":"59","author":"Tagliabue","year":"2010","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"4773","DOI":"10.1128\/jb.173.15.4773-4781.1991","article-title":"Purification and characterization of thin, aggregative fimbriae from","volume":"173","author":"Collinson","year":"1991","journal-title":"Salmonella Enteritidis J. Bacteriol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"D609","DOI":"10.1093\/nar\/gkae1010","article-title":"UniProt: The Universal Protein Knowledgebase in 2025","volume":"53","author":"UniProt","year":"2025","journal-title":"Nucleic Acids Res."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"2367","DOI":"10.1128\/AEM.67.5.2367-2370.2001","article-title":"Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157:H7","volume":"67","author":"Uhlich","year":"2001","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"D115","DOI":"10.1093\/nar\/gkh131","article-title":"Uniprot: The universal protein knowledgebase","volume":"32","author":"Apweiler","year":"2004","journal-title":"Nucleic Acids Res."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/9\/1932\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T11:56:13Z","timestamp":1788263773000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/14\/9\/1932"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,1]]},"references-count":86,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["microorganisms14091932"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms14091932","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,1]]}}}