{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,18]],"date-time":"2025-12-18T19:53:08Z","timestamp":1766087588093,"version":"3.41.2"},"reference-count":136,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2020,8,14]],"date-time":"2020-08-14T00:00:00Z","timestamp":1597363200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Nature Science Foundation of China","doi-asserted-by":"crossref","award":["61772313","11931008"],"award-info":[{"award-number":["61772313","11931008"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Interdisciplinary Science Innovation Group Project of Shandong University"},{"name":"Innovation Method Fund of China","award":["2018IM020200"],"award-info":[{"award-number":["2018IM020200"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,5,20]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Bacterial genomes are now recognized as interacting intimately with cellular processes. Uncovering organizational mechanisms of bacterial genomes has been a primary focus of researchers to reveal the potential cellular activities. The advances in both experimental techniques and computational models provide a tremendous opportunity for understanding these mechanisms, and various studies have been proposed to explore the organization rules of bacterial genomes associated with functions recently. This review focuses mainly on the principles that shape the organization of bacterial genomes, both locally and globally. We first illustrate local structures as operons\/transcription units for facilitating co-transcription and horizontal transfer of genes. We then clarify the constraints that globally shape bacterial genomes, such as metabolism, transcription and replication. Finally, we highlight challenges and opportunities to advance bacterial genomic studies and provide application perspectives of genome organization, including pathway hole assignment and genome assembly and understanding disease mechanisms.<\/jats:p>","DOI":"10.1093\/bib\/bbaa172","type":"journal-article","created":{"date-parts":[[2020,8,10]],"date-time":"2020-08-10T19:16:48Z","timestamp":1597087008000},"source":"Crossref","is-referenced-by-count":7,"title":["The functional determinants in the organization of bacterial genomes"],"prefix":"10.1093","volume":"22","author":[{"given":"Zhaoqian","family":"Liu","sequence":"first","affiliation":[{"name":"School of Mathematics, Shandong University"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jingtong","family":"Feng","sequence":"additional","affiliation":[{"name":"School of Mathematics, Shandong University"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2453-7852","authenticated-orcid":false,"given":"Bin","family":"Yu","sequence":"additional","affiliation":[{"name":"College of Mathematics and Physics, Qingdao University of Science and Technology"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qin","family":"Ma","sequence":"additional","affiliation":[{"name":"Department of Biomedical Informatics, the Ohio State University"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bingqiang","family":"Liu","sequence":"additional","affiliation":[{"name":"School of Mathematics, Shandong University"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2020,8,14]]},"reference":[{"key":"2021052110393631100_ref1","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1098\/rstb.2005.1758","article-title":"Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics","volume":"361","author":"Chater","year":"2006","journal-title":"Philos Trans R Soc B Biol Sci"},{"key":"2021052110393631100_ref2","doi-asserted-by":"crossref","first-page":"1378","DOI":"10.1038\/ismej.2014.222","article-title":"Bacterial community responses to a gradient of alkaline mountaintop mine drainage in central Appalachian streams","volume":"9","author":"Bier","year":"2015","journal-title":"ISME J"},{"key":"2021052110393631100_ref3","first-page":"1","article-title":"Single-cell bacterial transcription measurements reveal the importance of dimethylsulfoniopropionate (DMSP) hotspots in ocean sulfur cycling","volume":"11","author":"Gao","year":"2020","journal-title":"Nat Commun"},{"key":"2021052110393631100_ref4","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1007\/s00248-008-9431-6","article-title":"Antibiotic resistance in bacteria isolated from the deep terrestrial subsurface","volume":"57","author":"Brown","year":"2009","journal-title":"Microb Ecol"},{"key":"2021052110393631100_ref5","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1038\/nrendo.2016.150","article-title":"Role of the gut microbiota in host appetite control: bacterial growth to animal feeding behaviour","volume":"13","author":"Fetissov","year":"2017","journal-title":"Nat Rev Endocrinol"},{"volume-title":"Genome Size and Structure: Bacterial","year":"2016","author":"Ochman","key":"2021052110393631100_ref6"},{"key":"2021052110393631100_ref7","doi-asserted-by":"crossref","first-page":"72","DOI":"10.3389\/fgene.2017.00072","article-title":"The evolution of bacterial genome architecture","volume":"8","author":"Bobay","year":"2017","journal-title":"Front Genet"},{"key":"2021052110393631100_ref8","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1186\/1471-2164-15-721","article-title":"Overlapping genes: a window on gene evolvability","volume":"15","author":"Huvet","year":"2014","journal-title":"BMC Genomics"},{"key":"2021052110393631100_ref9","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1038\/nrmicro3380","article-title":"Molecular mechanisms of antibiotic resistance","volume":"13","author":"Blair","year":"2015","journal-title":"Nat Rev Microbiol"},{"key":"2021052110393631100_ref10","doi-asserted-by":"crossref","first-page":"S71","DOI":"10.1093\/cid\/ciu392","article-title":"The future of antibiotics and resistance: a tribute to a career of leadership by John Bartlett","volume":"59","author":"Spellberg","year":"2014","journal-title":"Clin Infect Dis"},{"key":"2021052110393631100_ref11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/MMBR.00035-13","article-title":"Bacterial genome instability","volume":"78","author":"Darmon","year":"2014","journal-title":"Microbiol Mol Biol Rev"},{"key":"2021052110393631100_ref12","first-page":"1727","article-title":"Operon: a group of genes with the expression coordinated by an operator","volume":"250","author":"Jacob","year":"1960","journal-title":"C R Hebd Seances Acad Sci"},{"key":"2021052110393631100_ref13","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1016\/S0022-2836(61)80072-7","article-title":"Genetic regulatory mechanisms in the synthesis of proteins","volume":"3","author":"Jacob","year":"1961","journal-title":"J Mol Biol"},{"key":"2021052110393631100_ref14","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.coisb.2018.02.007","article-title":"The organization of bacterial genomes: towards understanding the interplay between structure and function","volume":"8","author":"Brocken","year":"2018","journal-title":"Curr Opin Syst Biol"},{"key":"2021052110393631100_ref15","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1007\/s10142-015-0433-4","article-title":"Insights from 20 years of bacterial genome sequencing","volume":"15","author":"Land","year":"2015","journal-title":"Funct Integr Genomics"},{"key":"2021052110393631100_ref16","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1126\/science.270.5235.397","article-title":"The minimal gene complement of Mycoplasma genitalium","volume":"270","author":"Fraser","year":"1995","journal-title":"Science"},{"key":"2021052110393631100_ref17","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1126\/science.7542800","article-title":"Whole-genome random sequencing and assembly of Haemophilus influenzae Rd","volume":"269","author":"Fleischmann","year":"1995","journal-title":"Science"},{"key":"2021052110393631100_ref18","doi-asserted-by":"crossref","first-page":"1843","DOI":"10.1093\/genetics\/143.4.1843","article-title":"Selfish operons: horizontal transfer may drive the evolution of gene clusters","volume":"143","author":"Lawrence","year":"1996","journal-title":"Genetics"},{"key":"2021052110393631100_ref19","doi-asserted-by":"crossref","first-page":"6310","DOI":"10.1073\/pnas.0911237107","article-title":"Genomic arrangement of bacterial operons is constrained by biological pathways encoded in the genome","volume":"107","author":"Yin","year":"2010","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052110393631100_ref20","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/nsmb.2474","article-title":"Functional implications of genome topology","volume":"20","author":"Cavalli","year":"2013","journal-title":"Nat Struct Mol Biol"},{"key":"2021052110393631100_ref21","first-page":"1","article-title":"Chromosome organization in bacteria: mechanistic insights into genome structure and function","volume":"12","author":"Dame","year":"2019","journal-title":"Nat Rev Genet"},{"key":"2021052110393631100_ref22","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1146\/annurev.genet.42.110807.091653","article-title":"The organization of the bacterial genome","volume":"42","author":"Rocha","year":"2008","journal-title":"Annu Rev Genet"},{"key":"2021052110393631100_ref23","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.biocel.2008.09.015","article-title":"Evolution of genome architecture","volume":"41","author":"Koonin","year":"2009","journal-title":"Int J Biochem Cell Biol"},{"key":"2021052110393631100_ref24","doi-asserted-by":"crossref","first-page":"1902","DOI":"10.1093\/nar\/30.9.1902","article-title":"Pyrococcus genome comparison evidences chromosome shuffling-driven evolution","volume":"30","author":"Zivanovic","year":"2002","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref25","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.1126\/science.1455232","article-title":"Consequences of replication fork movement through transcription units in vivo","volume":"258","author":"French","year":"1992","journal-title":"Science"},{"key":"2021052110393631100_ref26","article-title":"Hi-C: a method to study the three-dimensional architecture of genomes","volume":"39","author":"Van Berkum","year":"2010","journal-title":"JoVE"},{"key":"2021052110393631100_ref27","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1038\/nrmicro2261","article-title":"Bacterial nucleoid-associated proteins, nucleoid structure and gene expression","volume":"8","author":"Dillon","year":"2010","journal-title":"Nat Rev Microbiol"},{"key":"2021052110393631100_ref28","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1111\/j.1365-2958.2005.04588.x","article-title":"Measuring chromosome dynamics on different time scales using resolvases with varying half-lives","volume":"56","author":"Stein","year":"2005","journal-title":"Mol Microbiol"},{"key":"2021052110393631100_ref29","doi-asserted-by":"crossref","first-page":"11383","DOI":"10.1093\/nar\/gku828","article-title":"Chromosome position effects on gene expression in Escherichia coli K-12","volume":"42","author":"Bryant","year":"2014","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref30","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1186\/1471-2164-9-559","article-title":"Differential replication dynamics for large and small vibrio chromosomes affect gene dosage, expression and location","volume":"9","author":"Dryselius","year":"2008","journal-title":"BMC Genomics"},{"key":"2021052110393631100_ref31","doi-asserted-by":"crossref","first-page":"5594","DOI":"10.1093\/nar\/gkt261","article-title":"Computational analyses of transcriptomic data reveal the dynamic organization of the Escherichia coli chromosome under different conditions","volume":"41","author":"Ma","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref32","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1101\/gad.14.2.212","article-title":"Dynamic organization of chromosomal DNA in Escherichia coli","volume":"14","author":"Niki","year":"2000","journal-title":"Genes Dev"},{"key":"2021052110393631100_ref33","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1002123","article-title":"Chromosomal macrodomains and associated proteins: implications for DNA organization and replication in gram negative bacteria","volume":"7","author":"Dame","year":"2011","journal-title":"PLoS Genet"},{"key":"2021052110393631100_ref34","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1101\/gr.200602","article-title":"Computational identification of operons in microbial genomes","volume":"12","author":"Zheng","year":"2002","journal-title":"Genome Res"},{"key":"2021052110393631100_ref35","first-page":"116","article-title":"A probabilistic learning approach to whole-genome operon prediction","volume":"8","author":"Craven","year":"2000","journal-title":"ISMB"},{"key":"2021052110393631100_ref36","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.1093\/nar\/29.5.1216","article-title":"Prediction of operons in microbial genomes","volume":"29","author":"Ermolaeva","year":"2001","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref37","doi-asserted-by":"crossref","first-page":"6652","DOI":"10.1073\/pnas.110147297","article-title":"Operons in Escherichia coli: genomic analyses and predictions","volume":"97","author":"Salgado","year":"2000","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052110393631100_ref38","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1093\/nar\/gkl1018","article-title":"Operon prediction using both genome-specific and general genomic information","volume":"35","author":"Dam","year":"2007","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref39","doi-asserted-by":"crossref","first-page":"D203","DOI":"10.1093\/nar\/gks1201","article-title":"RegulonDB v8. 0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more","volume":"41","author":"Salgado","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref40","doi-asserted-by":"crossref","first-page":"D93","DOI":"10.1093\/nar\/gkm910","article-title":"DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information","volume":"36","author":"Sierro","year":"2007","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref41","doi-asserted-by":"crossref","first-page":"D479","DOI":"10.1093\/nar\/gkn784","article-title":"OperonDB: a comprehensive database of predicted operons in microbial genomes","volume":"37","author":"Pertea","year":"2008","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref42","doi-asserted-by":"crossref","first-page":"D396","DOI":"10.1093\/nar\/gkp919","article-title":"MicrobesOnline: an integrated portal for comparative and functional genomics","volume":"38","author":"Dehal","year":"2010","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref43","doi-asserted-by":"crossref","first-page":"D358","DOI":"10.1093\/nar\/gkj037","article-title":"ODB: a database of operons accumulating known operons across multiple genomes","volume":"34","author":"Okuda","year":"2006","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref44","doi-asserted-by":"crossref","first-page":"D627","DOI":"10.1093\/nar\/gkr1020","article-title":"ProOpDB: prokaryotic operon data base","volume":"40","author":"Taboada","year":"2011","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref45","doi-asserted-by":"crossref","first-page":"D459","DOI":"10.1093\/nar\/gkn757","article-title":"DOOR: a database for prokaryotic operons","volume":"37","author":"Mao","year":"2008","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref46","doi-asserted-by":"crossref","first-page":"2586","DOI":"10.1093\/bioinformatics\/btx223","article-title":"DMINDA 2.0: integrated and systematic views of regulatory DNA motif identification and analyses","volume":"33","author":"Yang","year":"2017","journal-title":"Bioinformatics"},{"key":"2021052110393631100_ref47","doi-asserted-by":"crossref","first-page":"1568","DOI":"10.1093\/bib\/bbx088","article-title":"DOOR: a prokaryotic operon database for genome analyses and functional inference","volume":"20","author":"Cao","year":"2019","journal-title":"Brief Bioinform"},{"key":"2021052110393631100_ref48","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1111\/j.1365-2958.1994.tb00998.x","article-title":"The pdhR-aceEF-lpd operon of Escherichia coli expresses the pyruvate dehydrogenase complex","volume":"12","author":"Quail","year":"1994","journal-title":"Mol Microbiol"},{"key":"2021052110393631100_ref49","doi-asserted-by":"crossref","first-page":"3676","DOI":"10.1038\/s41467-018-05997-6","article-title":"SMRT-cappable-seq reveals complex operon variants in bacteria","volume":"9","author":"Yan","year":"2018","journal-title":"Nat Commun"},{"key":"2021052110393631100_ref50","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12859-015-0805-8","article-title":"Revisiting operons: an analysis of the landscape of transcriptional units in E. coli","volume":"16","author":"Mao","year":"2015","journal-title":"BMC Bioinformatics"},{"key":"2021052110393631100_ref51","doi-asserted-by":"crossref","first-page":"201","DOI":"10.3389\/fcimb.2019.00201","article-title":"Regulation of transcription termination of small RNAs and by small RNAs: molecular mechanisms and biological functions","volume":"9","author":"Chen","year":"2019","journal-title":"Front Cell Infect Microbiol"},{"key":"2021052110393631100_ref52","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1038\/nbt.1582","article-title":"The transcription unit architecture of the Escherichia coli genome","volume":"27","author":"Cho","year":"2009","journal-title":"Nat Biotechnol"},{"key":"2021052110393631100_ref53","doi-asserted-by":"crossref","first-page":"D654","DOI":"10.1093\/nar\/gkt1048","article-title":"DOOR 2.0: presenting operons and their functions through dynamic and integrated views","volume":"42","author":"Mao","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref54","doi-asserted-by":"crossref","first-page":"2827","DOI":"10.3389\/fmicb.2018.02827","article-title":"BAC-BROWSER: the tool for visualization and analysis of prokaryotic genomes","volume":"9","author":"Garanina","year":"2018","journal-title":"Front Microbiol"},{"key":"2021052110393631100_ref55","doi-asserted-by":"crossref","first-page":"e67","DOI":"10.1093\/nar\/gkv177","article-title":"Analysis of strand-specific RNA-seq data using machine learning reveals the structures of transcription units in Clostridium thermocellum","volume":"43","author":"Chou","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref56","first-page":"1","article-title":"SeqTU: a web server for identification of bacterial transcription units","volume":"7","author":"Chen","year":"2017","journal-title":"Sci Rep"},{"key":"2021052110393631100_ref57","doi-asserted-by":"crossref","first-page":"374","DOI":"10.3389\/fgene.2019.00374","article-title":"rSeqTU\u2014a machine-learning based R package for prediction of bacterial transcription units","volume":"10","author":"Niu","year":"2019","journal-title":"Front Genet"},{"key":"2021052110393631100_ref58","doi-asserted-by":"crossref","first-page":"13254","DOI":"10.1093\/nar\/gku976","article-title":"Transcriptome analysis reveals novel regulatory mechanisms in a genome-reduced bacterium","volume":"42","author":"Mazin","year":"2014","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref59","doi-asserted-by":"crossref","first-page":"2043","DOI":"10.1016\/j.febslet.2012.03.051","article-title":"The layout of a bacterial genome","volume":"586","author":"K\u00e9p\u00e8s","year":"2012","journal-title":"FEBS Lett"},{"key":"2021052110393631100_ref60","article-title":"Bacterial regulon modeling and prediction based on systematic cis regulatory motif analyses","volume":"6","author":"Liu","year":"2016","journal-title":"Sci Rep"},{"key":"2021052110393631100_ref61","article-title":"Genomic arrangement of regulons in bacterial genomes","volume":"7","author":"Zhang","year":"2012","journal-title":"PLoS One"},{"key":"2021052110393631100_ref62","doi-asserted-by":"crossref","first-page":"D394","DOI":"10.1093\/nar\/gkj156","article-title":"RegulonDB (version 5.0): Escherichia coli K-12 transcriptional regulatory network, operon organization, and growth conditions","volume":"34","author":"Salgado","year":"2006","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref63","doi-asserted-by":"crossref","first-page":"5691","DOI":"10.1093\/nar\/gki866","article-title":"The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes","volume":"33","author":"Overbeek","year":"2005","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref64","doi-asserted-by":"crossref","first-page":"D480","DOI":"10.1093\/nar\/gkm882","article-title":"KEGG for linking genomes to life and the environment","volume":"36","author":"Kanehisa","year":"2007","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref65","doi-asserted-by":"crossref","first-page":"6083","DOI":"10.1093\/nar\/gki892","article-title":"Expansion of the BioCyc collection of pathway\/genome databases to 160 genomes","volume":"33","author":"Karp","year":"2005","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref66","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1016\/j.gpb.2013.01.004","article-title":"Global genomic arrangement of bacterial genes is closely tied with the total transcriptional efficiency","volume":"11","author":"Ma","year":"2013","journal-title":"Genomics Proteomics Bioinformatics"},{"key":"2021052110393631100_ref67","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1126\/science.1242059","article-title":"High-resolution mapping of the spatial organization of a bacterial chromosome","volume":"342","author":"Le","year":"2013","journal-title":"Science"},{"key":"2021052110393631100_ref68","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1159\/000369098","article-title":"Dynamic organization: chromosome domains in Escherichia coli","volume":"24","author":"Messerschmidt","year":"2014","journal-title":"J Mol Microbiol Biotechnol"},{"key":"2021052110393631100_ref69","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a000349","article-title":"Bacterial chromosome organization and segregation","volume":"2","author":"Toro","year":"2010","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"2021052110393631100_ref70","doi-asserted-by":"crossref","DOI":"10.1186\/s12860-019-0211-6","article-title":"DNA supercoiling and transcription in bacteria: a two-way street","volume":"20","author":"Dorman","year":"2019","journal-title":"BMC Mol cell Biol"},{"key":"2021052110393631100_ref71","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1126\/science.227059","article-title":"A sign inversion mechanism for enzymatic supercoiling of DNA","volume":"206","author":"Brown","year":"1979","journal-title":"Science"},{"key":"2021052110393631100_ref72","doi-asserted-by":"crossref","first-page":"1104","DOI":"10.1073\/pnas.53.5.1104","article-title":"The twisted circular form of polyoma viral DNA","volume":"53","author":"Vinograd","year":"1965","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052110393631100_ref73","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1038\/nrmicro3007","article-title":"Genome architecture and global gene regulation in bacteria: making progress towards a unified model?","volume":"11","author":"Dorman","year":"2013","journal-title":"Nat Rev Microbiol"},{"key":"2021052110393631100_ref74","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1016\/j.cell.2017.11.032","article-title":"The biology of CRISPR-Cas: backward and forward","volume":"172","author":"Hille","year":"2018","journal-title":"Cell"},{"key":"2021052110393631100_ref75","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/nature09523","article-title":"The CRISPR\/Cas bacterial immune system cleaves bacteriophage and plasmid DNA","volume":"468","author":"Garneau","year":"2010","journal-title":"Nature"},{"key":"2021052110393631100_ref76","doi-asserted-by":"crossref","first-page":"6291","DOI":"10.1128\/JB.00644-10","article-title":"The Escherichia coli CRISPR system protects from \u03bb lysogenization, lysogens, and prophage induction","volume":"192","author":"Edgar","year":"2010","journal-title":"J Bacteriol"},{"key":"2021052110393631100_ref77","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.chom.2012.06.003","article-title":"CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection","volume":"12","author":"Bikard","year":"2012","journal-title":"Cell Host Microbe"},{"key":"2021052110393631100_ref78","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1038\/nature14302","article-title":"CRISPR adaptation biases explain preference for acquisition of foreign DNA","volume":"520","author":"Levy","year":"2015","journal-title":"Nature"},{"key":"2021052110393631100_ref79","doi-asserted-by":"crossref","first-page":"6260","DOI":"10.1073\/pnas.1819476116","article-title":"Interplay between DNA sequence and negative superhelicity drives R-loop structures","volume":"116","author":"Stolz","year":"2019","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052110393631100_ref80","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/j.molcel.2012.03.018","article-title":"CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3","volume":"46","author":"Westra","year":"2012","journal-title":"Mol Cell"},{"key":"2021052110393631100_ref81","doi-asserted-by":"crossref","first-page":"47564","DOI":"10.1074\/jbc.M403798200","article-title":"Coupling DNA supercoiling to transcription in defined protein systems","volume":"279","author":"Leng","year":"2004","journal-title":"J Biol Chem"},{"key":"2021052110393631100_ref82","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1016\/S0021-9258(17)42136-3","article-title":"Hypernegative supercoiling of the DNA template during transcription elongation in vitro","volume":"269","author":"Drolet","year":"1994","journal-title":"J Biol Chem"},{"key":"2021052110393631100_ref83","doi-asserted-by":"crossref","first-page":"1134","DOI":"10.4161\/rna.21410","article-title":"Cascade-mediated binding and bending of negatively supercoiled DNA","volume":"9","author":"Westra","year":"2012","journal-title":"RNA Biol"},{"key":"2021052110393631100_ref84","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1046\/j.1365-2958.2003.03461.x","article-title":"DNA supercoiling contributes to disconnect \u03c3S accumulation from \u03c3S-dependent transcription in Escherichia coli","volume":"48","author":"Bordes","year":"2003","journal-title":"Mol Microbiol"},{"key":"2021052110393631100_ref85","doi-asserted-by":"crossref","first-page":"134","DOI":"10.3390\/genes7120134","article-title":"The causes and consequences of topological stress during DNA replication","volume":"7","author":"Keszthelyi","year":"2016","journal-title":"Genes (Basel)"},{"key":"2021052110393631100_ref86","doi-asserted-by":"crossref","first-page":"972","DOI":"10.1093\/nar\/gkr779","article-title":"A model for Escherichia coli chromosome packaging supports transcription factor-induced DNA domain formation","volume":"40","author":"Fritsche","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref87","doi-asserted-by":"crossref","first-page":"291","DOI":"10.4161\/cib.4.3.14891","article-title":"Geometrical ordering of DNA in bacteria","volume":"4","author":"Buenemann","year":"2011","journal-title":"Commun Integr Biol"},{"key":"2021052110393631100_ref88","doi-asserted-by":"crossref","first-page":"9798","DOI":"10.1073\/pnas.1402597111","article-title":"Direct observation of R-loop formation by single RNA-guided Cas9 and Cascade effector complexes","volume":"111","author":"Szczelkun","year":"2014","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052110393631100_ref89","doi-asserted-by":"crossref","first-page":"7777","DOI":"10.1007\/s00253-016-7724-0","article-title":"Transcriptional analysis and adaptive evolution of Escherichia coli strains growing on acetate","volume":"100","author":"Rajaraman","year":"2016","journal-title":"Appl Microbiol Biotechnol"},{"key":"2021052110393631100_ref90","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1007\/s11427-014-4734-y","article-title":"Understanding the commonalities and differences in genomic organizations across closely related bacteria from an energy perspective","volume":"57","author":"Ma","year":"2014","journal-title":"Sci China Life Sci"},{"key":"2021052110393631100_ref91","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s00412-016-0593-6","article-title":"Chromosome organization in bacteria: mechanistic understanding genome function","volume":"126","author":"Sati","year":"2017","journal-title":"Chromosoma"},{"key":"2021052110393631100_ref92","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1038\/ng1891","article-title":"Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra-and interchromosomal interactions","volume":"38","author":"Zhao","year":"2006","journal-title":"Nat Genet"},{"key":"2021052110393631100_ref93","doi-asserted-by":"crossref","first-page":"D212","DOI":"10.1093\/nar\/gky1077","article-title":"RegulonDB v 10.5: tackling challenges to unify classic and high throughput knowledge of gene regulation in E. coli K-12","volume":"47","author":"Santos-Zavaleta","year":"2019","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref94","doi-asserted-by":"crossref","first-page":"1561","DOI":"10.1042\/BST20160190","article-title":"Structure and function of bacterial H-NS protein","volume":"44","author":"Grainger","year":"2016","journal-title":"Biochem Soc Trans"},{"key":"2021052110393631100_ref95","doi-asserted-by":"crossref","first-page":"2073","DOI":"10.1093\/nar\/gkq934","article-title":"Direct and indirect effects of H-NS and Fis on global gene expression control in Escherichia coli","volume":"39","author":"Kahramanoglou","year":"2011","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref96","doi-asserted-by":"crossref","first-page":"4642","DOI":"10.1093\/nar\/gkl542","article-title":"Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome","volume":"34","author":"Grainger","year":"2006","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref97","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/S1097-2765(03)00108-4","article-title":"Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners","volume":"11","author":"Schleiffer","year":"2003","journal-title":"Mol Cell"},{"key":"2021052110393631100_ref98","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1111\/1574-6976.12045","article-title":"The bacterial chromosome: architecture and action of bacterial SMC and SMC-like complexes","volume":"38","author":"Nolivos","year":"2014","journal-title":"FEMS Microbiol Rev"},{"key":"2021052110393631100_ref99","doi-asserted-by":"crossref","first-page":"2183","DOI":"10.1016\/j.str.2015.10.004","article-title":"Kite proteins: a superfamily of SMC\/Kleisin partners conserved across bacteria, archaea, and eukaryotes","volume":"23","author":"Palecek","year":"2015","journal-title":"Structure"},{"key":"2021052110393631100_ref100","doi-asserted-by":"crossref","first-page":"4067","DOI":"10.1128\/JB.00010-10","article-title":"Contribution of SMC (structural maintenance of chromosomes) and spoIIIE to chromosome segregation in staphylococci","volume":"192","author":"Yu","year":"2010","journal-title":"J Bacteriol"},{"key":"2021052110393631100_ref101","doi-asserted-by":"crossref","first-page":"11202","DOI":"10.1093\/nar\/gks925","article-title":"Self-organization of domain structures by DNA-loop-extruding enzymes","volume":"40","author":"Alipour","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref102","doi-asserted-by":"crossref","first-page":"1595","DOI":"10.1083\/jcb.142.6.1595","article-title":"The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge","volume":"142","author":"Melby","year":"1998","journal-title":"J Cell Biol"},{"key":"2021052110393631100_ref103","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1038\/nrm.2016.30","article-title":"SMC complexes: from DNA to chromosomes","volume":"17","author":"Uhlmann","year":"2016","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2021052110393631100_ref104","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0150189","article-title":"DNA sequence determinants controlling affinity, stability and shape of DNA complexes bound by the nucleoid protein Fis","volume":"11","author":"Hancock","year":"2016","journal-title":"PLoS One"},{"key":"2021052110393631100_ref105","doi-asserted-by":"crossref","first-page":"11156","DOI":"10.1093\/nar\/gku804","article-title":"Direct regulation of topoisomerase activity by a nucleoid-associated protein","volume":"42","author":"Ghosh","year":"2014","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref106","doi-asserted-by":"crossref","first-page":"1297","DOI":"10.1016\/j.celrep.2015.02.004","article-title":"Comparative hi-C reveals that CTCF underlies evolution of chromosomal domain architecture","volume":"10","author":"Vietri Rudan","year":"2015","journal-title":"Cell Rep"},{"key":"2021052110393631100_ref107","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/ncomms11055","article-title":"Genome scale patterns of supercoiling in a bacterial chromosome","volume":"7","author":"Lal","year":"2016","journal-title":"Nat Commun"},{"key":"2021052110393631100_ref108","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1038\/nature11082","article-title":"Topological domains in mammalian genomes identified by analysis of chromatin interactions","volume":"485","author":"Dixon","year":"2012","journal-title":"Nature"},{"key":"2021052110393631100_ref109","doi-asserted-by":"crossref","first-page":"1582","DOI":"10.15252\/embj.201593561","article-title":"Transcription rate and transcript length drive formation of chromosomal interaction domain boundaries","volume":"35","author":"Le","year":"2016","journal-title":"EMBO J"},{"key":"2021052110393631100_ref110","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1101\/gr.196006.115","article-title":"Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains","volume":"26","author":"Ulianov","year":"2016","journal-title":"Genome Res"},{"key":"2021052110393631100_ref111","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1016\/j.cell.2017.12.027","article-title":"Multiscale structuring of the E. coli chromosome by nucleoid-associated and condensin proteins","volume":"172","author":"Lioy","year":"2018","journal-title":"Cell"},{"key":"2021052110393631100_ref112","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1016\/S0092-8674(00)81909-1","article-title":"Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis","volume":"88","author":"Webb","year":"1997","journal-title":"Cell"},{"key":"2021052110393631100_ref113","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1002672","article-title":"Long-range chromosome organization in E. coli: a site-specific system isolates the ter macrodomain","volume":"8","author":"Thiel","year":"2012","journal-title":"PLoS Genet"},{"key":"2021052110393631100_ref114","doi-asserted-by":"crossref","first-page":"1418","DOI":"10.1111\/j.1365-2958.2008.06239.x","article-title":"DNA dynamics vary according to macrodomain topography in the E. coli chromosome","volume":"68","author":"Espeli","year":"2008","journal-title":"Mol Microbiol"},{"key":"2021052110393631100_ref115","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pgen.1006758","article-title":"Long range chromosome organization in Escherichia coli: the position of the replication origin defines the non-structured regions and the right and left macrodomains","volume":"13","author":"Duigou","year":"2017","journal-title":"PLoS Genet"},{"key":"2021052110393631100_ref116","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms3003","article-title":"Short-time movement of E. coli chromosomal loci depends on coordinate and subcellular localization","volume":"4","author":"Javer","year":"2013","journal-title":"Nat Commun"},{"key":"2021052110393631100_ref117","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pgen.1006309","article-title":"The MaoP\/maoS site-specific system organizes the Ori region of the E. coli chromosome into a macrodomain","volume":"12","author":"Valens","year":"2016","journal-title":"PLoS Genet"},{"key":"2021052110393631100_ref118","first-page":"1","article-title":"Selection for energy efficiency drives strand-biased gene distribution in prokaryotes","volume":"7","author":"Gao","year":"2017","journal-title":"Sci Rep"},{"key":"2021052110393631100_ref119","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1038\/ng1209","article-title":"Essentiality, not expressiveness, drives gene-strand bias in bacteria","volume":"34","author":"Rocha","year":"2003","journal-title":"Nat Genet"},{"key":"2021052110393631100_ref120","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1016\/0092-8674(88)90086-4","article-title":"When polymerases collide: replication and the transcriptional organization of the E. coli chromosome","volume":"53","author":"Brewer","year":"1988","journal-title":"Cell"},{"key":"2021052110393631100_ref121","doi-asserted-by":"crossref","first-page":"8210","DOI":"10.1093\/nar\/gks605","article-title":"The percentage of bacterial genes on leading versus lagging strands is influenced by multiple balancing forces","volume":"40","author":"Mao","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref122","doi-asserted-by":"crossref","first-page":"3788","DOI":"10.1093\/emboj\/19.14.3788","article-title":"Role of ribosome recycling factor (RRF) in translational coupling","volume":"19","author":"Inokuchi","year":"2000","journal-title":"EMBO J"},{"key":"2021052110393631100_ref123","doi-asserted-by":"crossref","first-page":"e150","DOI":"10.1093\/nar\/gkr766","article-title":"Integration of sequence-similarity and functional association information can overcome intrinsic problems in orthology mapping across bacterial genomes","volume":"39","author":"Li","year":"2011","journal-title":"Nucleic Acids Res"},{"key":"2021052110393631100_ref124","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1042\/BJ20091328","article-title":"Unknown\u2019proteins and \u2018orphan\u2019enzymes: the missing half of the engineering parts list\u2013and how to find it","volume":"425","author":"Hanson","year":"2010","journal-title":"Biochem J"},{"key":"2021052110393631100_ref125","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1038\/nmeth.1527","article-title":"Limitations of next-generation genome sequence assembly","volume":"8","author":"Alkan","year":"2011","journal-title":"Nat Methods"},{"key":"2021052110393631100_ref126","doi-asserted-by":"crossref","first-page":"2443","DOI":"10.1093\/bioinformatics\/btv171","article-title":"MeDuSa: a multi-draft based scaffolder","volume":"31","author":"Bosi","year":"2015","journal-title":"Bioinformatics"},{"key":"2021052110393631100_ref127","doi-asserted-by":"crossref","first-page":"i319","DOI":"10.1093\/bioinformatics\/btu291","article-title":"AlignGraph: algorithm for secondary de novo genome assembly guided by closely related references","volume":"30","author":"Bao","year":"2014","journal-title":"Bioinformatics"},{"key":"2021052110393631100_ref128","doi-asserted-by":"crossref","first-page":"1785","DOI":"10.1073\/pnas.1220349110","article-title":"Reference-assisted chromosome assembly","volume":"110","author":"Kim","year":"2013","journal-title":"Proc Natl Acad Sci USA"},{"key":"2021052110393631100_ref129","doi-asserted-by":"crossref","first-page":"R101","DOI":"10.1186\/gb-2013-14-9-r101","article-title":"Reducing assembly complexity of microbial genomes with single-molecule sequencing","volume":"14","author":"Koren","year":"2013","journal-title":"Genome Biol"},{"key":"2021052110393631100_ref130","doi-asserted-by":"crossref","first-page":"e01867","DOI":"10.1128\/mBio.01867-14","article-title":"Flexibility and symmetry of prokaryotic genome rearrangement reveal lineage-associated core-gene-defined genome organizational frameworks","volume":"5","author":"Kang","year":"2014","journal-title":"MBio"},{"key":"2021052110393631100_ref131","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12864-016-3267-0","article-title":"GAAP: genome-organization-framework-assisted assembly pipeline for prokaryotic genomes","volume":"18","author":"Yuan","year":"2017","journal-title":"BMC Genomics"},{"key":"2021052110393631100_ref132","article-title":"Probing the mobilome: discoveries in the dynamic microbiome","author":"Carr","year":"2020","journal-title":"Trends Microbiol"},{"key":"2021052110393631100_ref133","doi-asserted-by":"publisher","DOI":"10.1093\/bib\/bbaa005","article-title":"Network analyses in microbiome based on high-throughput multi-omics data","author":"Liu","year":"2020","journal-title":"Brief Bioinform"},{"key":"2021052110393631100_ref134","article-title":"The gut microbiota: emerging evidence in autoimmune diseases","author":"Zhang","year":"2020","journal-title":"Trends Mol Med"},{"key":"2021052110393631100_ref135","doi-asserted-by":"crossref","DOI":"10.1038\/srep43772","article-title":"The alr-groEL1 operon in mycobacterium tuberculosis: an interplay of multiple regulatory elements","volume":"7","author":"Bhat","year":"2017","journal-title":"Sci Rep"},{"key":"2021052110393631100_ref136","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1038\/nature08756","article-title":"The primary transcriptome of the major human pathogen Helicobacter pylori","volume":"464","author":"Sharma","year":"2010","journal-title":"Nature"}],"container-title":["Briefings in Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/bib\/article-pdf\/22\/3\/bbaa172\/37964937\/bbaa172.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/bib\/article-pdf\/22\/3\/bbaa172\/37964937\/bbaa172.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,6]],"date-time":"2022-11-06T12:00:31Z","timestamp":1667736031000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bib\/article\/doi\/10.1093\/bib\/bbaa172\/5892344"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,14]]},"references-count":136,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2021,5,20]]}},"URL":"https:\/\/doi.org\/10.1093\/bib\/bbaa172","relation":{},"ISSN":["1467-5463","1477-4054"],"issn-type":[{"type":"print","value":"1467-5463"},{"type":"electronic","value":"1477-4054"}],"subject":[],"published-other":{"date-parts":[[2021,5]]},"published":{"date-parts":[[2020,8,14]]},"article-number":"bbaa172"}}