{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T23:31:38Z","timestamp":1793316698837,"version":"4.5.0"},"reference-count":50,"publisher":"Springer Science and Business Media LLC","issue":"8027","license":[{"start":{"date-parts":[[2024,7,31]],"date-time":"2024-07-31T00:00:00Z","timestamp":1722384000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,7,31]],"date-time":"2024-07-31T00:00:00Z","timestamp":1722384000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nature"],"published-print":{"date-parts":[[2024,8,29]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Exposure to environmental pollutants and human microbiome composition are important predisposition factors for tumour development\n                    <jats:sup>1,2<\/jats:sup>\n                    . Similar to drug molecules, pollutants are typically metabolized in the body, which can change their carcinogenic potential and affect tissue distribution through altered toxicokinetics\n                    <jats:sup>3<\/jats:sup>\n                    . Although recent studies demonstrated that human-associated microorganisms can chemically convert a wide range of xenobiotics and influence the profile and tissue exposure of resulting metabolites\n                    <jats:sup>4,5<\/jats:sup>\n                    , the effect of microbial biotransformation on chemical-induced tumour development remains unclear. Here we show that the depletion of the gut microbiota affects the toxicokinetics of nitrosamines, which markedly reduces the development and severity of nitrosamine-induced urinary bladder cancer in mice\n                    <jats:sup>6,7<\/jats:sup>\n                    . We causally linked this carcinogen biotransformation to specific gut bacterial isolates in vitro and in vivo using individualized bacterial culture collections and gnotobiotic mouse models, respectively. We tested gut communities from different human donors to demonstrate that microbial carcinogen metabolism varies between individuals and we showed that this metabolic activity applies to structurally related nitrosamine carcinogens. Altogether, these results indicate that gut microbiota carcinogen metabolism may be a contributing factor for chemical-induced carcinogenesis, which could open avenues to target the microbiome for improved predisposition risk assessment and prevention of cancer.\n                  <\/jats:p>","DOI":"10.1038\/s41586-024-07754-w","type":"journal-article","created":{"date-parts":[[2024,7,31]],"date-time":"2024-07-31T12:07:06Z","timestamp":1722427626000},"page":"1137-1144","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":116,"title":["Gut microbiota carcinogen metabolism causes distal tissue tumours"],"prefix":"10.1038","volume":"632","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3168-9010","authenticated-orcid":false,"given":"Blanka","family":"Roje","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2856-9376","authenticated-orcid":false,"given":"Boyao","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2127-4150","authenticated-orcid":false,"given":"Eleonora","family":"Mastrorilli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7857-1549","authenticated-orcid":false,"given":"Ana","family":"Kova\u010di\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lana","family":"Su\u0161ak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivica","family":"Ljubenkov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena","family":"\u0106osi\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katarina","family":"Vilovi\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0156-2748","authenticated-orcid":false,"given":"Antonio","family":"Me\u0161trovi\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emilija Lozo","family":"Vukovac","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Viljemka","family":"Bu\u010devi\u0107-Popovi\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"\u017deljko","family":"Puljiz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivana","family":"Karaman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3228-2076","authenticated-orcid":false,"given":"Jano\u0161","family":"Terzi\u0107","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5797-3589","authenticated-orcid":false,"given":"Michael","family":"Zimmermann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,7,31]]},"reference":[{"key":"7754_CR1","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1158\/2159-8290.CD-21-1059","volume":"12","author":"D Hanahan","year":"2022","unstructured":"Hanahan, D. Hallmarks of cancer: new dimensions. Cancer Discov. 12, 31\u201346 (2022).","journal-title":"Cancer Discov."},{"key":"7754_CR2","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1016\/j.cell.2021.01.043","volume":"184","author":"A Peters","year":"2021","unstructured":"Peters, A., Nawrot, T. S. & Baccarelli, A. A. Hallmarks of environmental insults. Cell 184, 1455\u20131468 (2021).","journal-title":"Cell"},{"key":"7754_CR3","doi-asserted-by":"crossref","first-page":"1316","DOI":"10.1021\/tx300132k","volume":"25","author":"S Rendic","year":"2012","unstructured":"Rendic, S. & Guengerich, F. P. Contributions of human enzymes in carcinogen metabolism. Chem. Res. Toxicol. 25, 1316\u20131383 (2012).","journal-title":"Chem. Res. Toxicol."},{"key":"7754_CR4","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1038\/s41586-019-1291-3","volume":"570","author":"M Zimmermann","year":"2019","unstructured":"Zimmermann, M., Zimmermann-Kogadeeva, M., Wegmann, R. & Goodman, A. L. Mapping human microbiome drug metabolism by gut bacteria and their genes. Nature 570, 462\u2013467 (2019).","journal-title":"Nature"},{"key":"7754_CR5","doi-asserted-by":"crossref","first-page":"eaat9931","DOI":"10.1126\/science.aat9931","volume":"363","author":"M Zimmermann","year":"2019","unstructured":"Zimmermann, M., Zimmermann-Kogadeeva, M., Wegmann, R. & Goodman, A. L. Separating host and microbiome contributions to drug pharmacokinetics and toxicity. Science 363, eaat9931 (2019).","journal-title":"Science"},{"key":"7754_CR6","first-page":"727","volume":"26","author":"C Vasconcelos-N\u00f3brega","year":"2012","unstructured":"Vasconcelos-N\u00f3brega, C., Cola\u00e7o, A., Lopes, C. & Oliveira, P. A. BBN as an urothelial carcinogen. In Vivo 26, 727\u2013739 (2012).","journal-title":"In Vivo"},{"key":"7754_CR7","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.mrgentox.2011.11.015","volume":"742","author":"Z He","year":"2012","unstructured":"He, Z., Kosinska, W., Zhao, Z.-L., Wu, X.-R. & Guttenplan, J. B. Tissue-specific mutagenesis by N-butyl-N-(4-hydroxybutyl)nitrosamine as the basis for urothelial carcinogenesis. Mutat. Res. 742, 92\u201395 (2012).","journal-title":"Mutat. Res."},{"key":"7754_CR8","volume":"371","author":"GD Sepich-Poore","year":"2021","unstructured":"Sepich-Poore, G. D. et al. The microbiome and human cancer. Science 371, eabc4552 (2021).","journal-title":"Science"},{"key":"7754_CR9","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1038\/s41591-019-0377-7","volume":"25","author":"BA Helmink","year":"2019","unstructured":"Helmink, B. A., Khan, M. A. W., Hermann, A., Gopalakrishnan, V. & Wargo, J. A. The microbiome, cancer, and cancer therapy. Nat. Med. 25, 377\u2013388 (2019).","journal-title":"Nat. Med."},{"key":"7754_CR10","doi-asserted-by":"crossref","first-page":"973","DOI":"10.1126\/science.aay9189","volume":"368","author":"D Nejman","year":"2020","unstructured":"Nejman, D. et al. The human tumor microbiome is composed of tumor type\u2013specific intracellular bacteria. Science 368, 973\u2013980 (2020).","journal-title":"Science"},{"key":"7754_CR11","doi-asserted-by":"crossref","DOI":"10.1126\/science.aav9000","volume":"363","author":"MR Wilson","year":"2019","unstructured":"Wilson, M. R. et al. The human gut bacterial genotoxin colibactin alkylates DNA. Science 363, eaar7785 (2019).","journal-title":"Science"},{"key":"7754_CR12","first-page":"2979","volume":"56","author":"T Shimada","year":"1996","unstructured":"Shimada, T. et al. Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56, 2979\u20132984 (1996).","journal-title":"Cancer Res."},{"key":"7754_CR13","doi-asserted-by":"crossref","first-page":"394","DOI":"10.3322\/caac.21492","volume":"68","author":"F Bray","year":"2018","unstructured":"Bray, F. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 68, 394\u2013424 (2018).","journal-title":"CA Cancer J. Clin."},{"key":"7754_CR14","doi-asserted-by":"crossref","first-page":"S34","DOI":"10.1038\/551S34a","volume":"551","author":"C Berdik","year":"2017","unstructured":"Berdik, C. Unlocking bladder cancer. Nature 551, S34\u2013S35 (2017).","journal-title":"Nature"},{"key":"7754_CR15","first-page":"3666","volume":"48","author":"M Bonfanti","year":"1988","unstructured":"Bonfanti, M., Magagnotti, C., Bonati, M., Fanelli, R. & Airoldi, L. Pharmacokinetic profile and metabolism of N-nitrosobutyl-(4-hydroxybutyl)amine in rats. Cancer Res. 48, 3666\u20133669 (1988).","journal-title":"Cancer Res."},{"key":"7754_CR16","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1016\/j.str.2017.05.003","volume":"25","author":"RM Pollet","year":"2017","unstructured":"Pollet, R. M. et al. An atlas of \u03b2-glucuronidases in the human intestinal microbiome. Structure 25, 967\u2013977 (2017).","journal-title":"Structure"},{"key":"7754_CR17","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-018-34678-z","volume":"8","author":"P Dashnyam","year":"2018","unstructured":"Dashnyam, P. et al. \u03b2-Glucuronidases of opportunistic bacteria are the major contributors to xenobiotic-induced toxicity in the gut. Sci. Rep. 8, 16372 (2018).","journal-title":"Sci. Rep."},{"key":"7754_CR18","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1093\/jat\/29.6.570","volume":"29","author":"MA ElSohly","year":"2005","unstructured":"ElSohly, M. A., Gul, W., Feng, S. & Murphy, T. P. Hydrolysis of conjugated metabolites of buprenorphine II. The quantitative enzymatic hydrolysis of norbuprenorphine-3-\u03b2-D-glucuronide in human urine. J. Anal. Toxicol. 29, 570\u2013573 (2005).","journal-title":"J. Anal. Toxicol."},{"key":"7754_CR19","volume":"1","author":"I Lagkouvardos","year":"2016","unstructured":"Lagkouvardos, I. et al. The Mouse Intestinal Bacterial Collection (miBC) provides host-specific insight into cultured diversity and functional potential of the gut microbiota. Nat. Microbiol. 1, 16131 (2016).","journal-title":"Nat. Microbiol."},{"key":"7754_CR20","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s00018-017-2693-8","volume":"75","author":"F Hugenholtz","year":"2018","unstructured":"Hugenholtz, F. & de Vos, W. M. Mouse models for human intestinal microbiota research: a critical evaluation. Cell. Mol. Life Sci. 75, 149\u2013160 (2018).","journal-title":"Cell. Mol. Life Sci."},{"key":"7754_CR21","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.31035","volume":"6","author":"M Galardini","year":"2017","unstructured":"Galardini, M. et al. Phenotype inference in an Escherichia coli strain panel. Elife 6, e31035 (2017).","journal-title":"Elife"},{"key":"7754_CR22","first-page":"825","volume":"67","author":"M Okada","year":"1976","unstructured":"Okada, M., Suzuki, E. & Hashimoto, Y. Carcinogenicity of N-nitrosamines related to N-butyl-N-(4-hydroxybutyl)nitrosamine and N,N-dibutylnitrosamine in ACI\/N rats. GANN. Jpn. J. Cancer Res. 67, 825\u2013834 (1976).","journal-title":"Jpn. J. Cancer Res."},{"key":"7754_CR23","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1038\/nature11465","volume":"491","author":"SI Grivennikov","year":"2012","unstructured":"Grivennikov, S. I. et al. Adenoma-linked barrier defects and microbial products drive IL-23\/IL\u221217-mediated tumour growth. Nature 491, 254\u2013258 (2012).","journal-title":"Nature"},{"key":"7754_CR24","doi-asserted-by":"crossref","DOI":"10.1186\/s12967-019-02146-5","volume":"17","author":"M Degoricija","year":"2019","unstructured":"Degoricija, M. et al. The dynamics of the inflammatory response during BBN-induced bladder carcinogenesis in mice. J. Transl. Med. 17, 394 (2019).","journal-title":"J. Transl. Med."},{"key":"7754_CR25","first-page":"3806","volume":"58","author":"K Ozaki","year":"1998","unstructured":"Ozaki, K. et al. High susceptibility of p53(+\/-) knockout mice in N-butyl-N-(4-hydroxybutyl)nitrosamine urinary bladder carcinogenesis and lack of frequent mutation in residual allele. Cancer Res. 58, 3806\u20133811 (1998).","journal-title":"Cancer Res."},{"key":"7754_CR26","doi-asserted-by":"crossref","first-page":"1781","DOI":"10.1136\/gutjnl-2018-317715","volume":"68","author":"F Hildebrand","year":"2019","unstructured":"Hildebrand, F. et al. Antibiotics-induced monodominance of a novel gut bacterial order. Gut 68, 1781 (2019).","journal-title":"Gut"},{"key":"7754_CR27","doi-asserted-by":"crossref","first-page":"4516","DOI":"10.1073\/pnas.1000080107","volume":"108","author":"JG Caporaso","year":"2011","unstructured":"Caporaso, J. G. et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl Acad. Sci. USA 108, 4516 (2011).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"7754_CR28","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1038\/s41587-019-0209-9","volume":"37","author":"E Bolyen","year":"2019","unstructured":"Bolyen, E. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 37, 852\u2013857 (2019).","journal-title":"Nat. Biotechnol."},{"key":"7754_CR29","doi-asserted-by":"crossref","first-page":"1138","DOI":"10.1089\/cmb.2017.0096","volume":"24","author":"A Kechin","year":"2017","unstructured":"Kechin, A., Boyarskikh, U., Kel, A. & Filipenko, M. cutPrimers: a new tool for accurate cutting of primers from reads of targeted next generation sequencing. J. Comput. Biol. 24, 1138\u20131143 (2017).","journal-title":"J. Comput. Biol."},{"key":"7754_CR30","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nmeth.3869","volume":"13","author":"BJ Callahan","year":"2016","unstructured":"Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581\u2013583 (2016).","journal-title":"Nat. Methods"},{"key":"7754_CR31","doi-asserted-by":"crossref","first-page":"e00021-18","DOI":"10.1128\/mSystems.00021-18","volume":"3","author":"S Janssen","year":"2018","unstructured":"Janssen, S. et al. Phylogenetic placement of exact amplicon sequences improves associations with clinical information. Msystems 3, e00021-18 (2018).","journal-title":"Msystems"},{"key":"7754_CR32","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1093\/bioinformatics\/bts252","volume":"28","author":"E Pruesse","year":"2012","unstructured":"Pruesse, E., Peplies, J. & Gl\u00f6ckner, F. O. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics 28, 1823\u20131829 (2012).","journal-title":"Bioinformatics"},{"key":"7754_CR33","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","volume":"215","author":"SF Altschul","year":"1990","unstructured":"Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403\u2013410 (1990).","journal-title":"J. Mol. Biol."},{"key":"7754_CR34","doi-asserted-by":"crossref","first-page":"e2584","DOI":"10.7717\/peerj.2584","volume":"4","author":"T Rognes","year":"2016","unstructured":"Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mah\u00e9, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).","journal-title":"PeerJ"},{"key":"7754_CR35","doi-asserted-by":"crossref","DOI":"10.1186\/s40168-018-0470-z","volume":"6","author":"NA Bokulich","year":"2018","unstructured":"Bokulich, N. A. et al. Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2\u2019s q2-feature-classifier plugin. Microbiome 6, 90 (2018).","journal-title":"Microbiome"},{"key":"7754_CR36","doi-asserted-by":"crossref","first-page":"3059","DOI":"10.1093\/nar\/gkf436","volume":"30","author":"K Katoh","year":"2002","unstructured":"Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059\u20133066 (2002).","journal-title":"Nucleic Acids Res."},{"key":"7754_CR37","doi-asserted-by":"crossref","first-page":"e9490","DOI":"10.1371\/journal.pone.0009490","volume":"5","author":"MN Price","year":"2010","unstructured":"Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2 \u2013 approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).","journal-title":"PLoS ONE"},{"key":"7754_CR38","doi-asserted-by":"crossref","first-page":"W256","DOI":"10.1093\/nar\/gkz239","volume":"47","author":"I Letunic","year":"2019","unstructured":"Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256\u2013W259 (2019).","journal-title":"Nucleic Acids Res."},{"key":"7754_CR39","unstructured":"Andrews, S. FastQC: a quality control tool for high throughput sequence data (Babraham Bioinformatics, 2010); https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"7754_CR40","doi-asserted-by":"crossref","first-page":"3047","DOI":"10.1093\/bioinformatics\/btw354","volume":"32","author":"P Ewels","year":"2016","unstructured":"Ewels, P., Magnusson, M., Lundin, S. & K\u00e4ller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047\u20133048 (2016).","journal-title":"Bioinformatics"},{"key":"7754_CR41","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","volume":"30","author":"AM Bolger","year":"2014","unstructured":"Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114 (2014). 2120.","journal-title":"Bioinformatics"},{"key":"7754_CR42","doi-asserted-by":"crossref","first-page":"e102","DOI":"10.1002\/cpbi.102","volume":"70","author":"A Prjibelski","year":"2020","unstructured":"Prjibelski, A., Antipov, D., Meleshko, D., Lapidus, A., & Korobeynikov, A. Using SPAdes de novo assembler. Curr. Protoc. Bioinform. 70, e102 (2020).","journal-title":"Curr. Protoc. Bioinform."},{"key":"7754_CR43","doi-asserted-by":"crossref","first-page":"i142","DOI":"10.1093\/bioinformatics\/bty266","volume":"34","author":"A Mikheenko","year":"2018","unstructured":"Mikheenko, A., Prjibelski, A., Saveliev, V., Antipov, D. & Gurevich, A. Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 34, i142\u2013i150 (2018).","journal-title":"Bioinformatics"},{"key":"7754_CR44","volume":"20","author":"DE Wood","year":"2019","unstructured":"Wood, D. E., Lu, J. & Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 20, 257 (2019).","journal-title":"Genome Biol."},{"key":"7754_CR45","doi-asserted-by":"crossref","first-page":"5315","DOI":"10.1093\/bioinformatics\/btac672","volume":"38","author":"P-A Chaumeil","year":"2022","unstructured":"Chaumeil, P.-A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk v2: memory friendly classification with the genome taxonomy database. Bioinformatics 38, 5315\u20135316 (2022).","journal-title":"Bioinformatics"},{"key":"7754_CR46","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1093\/bioinformatics\/btab465","volume":"38","author":"G Salazar","year":"2021","unstructured":"Salazar, G., Ruscheweyh, H.-J., Hildebrand, F., Acinas, S. G. & Sunagawa, S. mTAGs: taxonomic profiling using degenerate consensus reference sequences of ribosomal RNA genes. Bioinformatics 38, 270\u2013272 (2021).","journal-title":"Bioinformatics"},{"key":"7754_CR47","doi-asserted-by":"crossref","first-page":"2068","DOI":"10.1093\/bioinformatics\/btu153","volume":"30","author":"T Seemann","year":"2014","unstructured":"Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068\u20132069 (2014).","journal-title":"Bioinformatics"},{"key":"7754_CR48","doi-asserted-by":"crossref","first-page":"3691","DOI":"10.1093\/bioinformatics\/btv421","volume":"31","author":"AJ Page","year":"2015","unstructured":"Page, A. J. et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691\u20133693 (2015).","journal-title":"Bioinformatics"},{"key":"7754_CR49","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1093\/bioinformatics\/btx610","volume":"34","author":"J Hadfield","year":"2017","unstructured":"Hadfield, J. et al. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics 34, 292\u2013293 (2017).","journal-title":"Bioinformatics"},{"key":"7754_CR50","doi-asserted-by":"crossref","first-page":"W293","DOI":"10.1093\/nar\/gkab301","volume":"49","author":"I Letunic","year":"2021","unstructured":"Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293\u2013W296 (2021).","journal-title":"Nucleic Acids Res."}],"container-title":["Nature"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07754-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07754-w","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07754-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,8,28]],"date-time":"2024-08-28T09:13:44Z","timestamp":1724836424000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41586-024-07754-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,7,31]]},"references-count":50,"journal-issue":{"issue":"8027","published-print":{"date-parts":[[2024,8,29]]}},"alternative-id":["7754"],"URL":"https:\/\/doi.org\/10.1038\/s41586-024-07754-w","relation":{},"ISSN":["0028-0836","1476-4687"],"issn-type":[{"value":"0028-0836","type":"print"},{"value":"1476-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,31]]},"assertion":[{"value":"30 January 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 June 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"31 July 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}