{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T19:41:55Z","timestamp":1790019715069,"version":"4.0.1"},"reference-count":93,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2024,11,16]],"date-time":"2024-11-16T00:00:00Z","timestamp":1731715200000},"content-version":"vor","delay-in-days":46,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"name":"National Institute for Allergy and Infectious Diseases","award":["R01AI105185"],"award-info":[{"award-number":["R01AI105185"]}]},{"name":"National Institute for Allergy and Infectious Diseases","award":["R01AI163202"],"award-info":[{"award-number":["R01AI163202"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Orphan DNA adenine methyltransferases (MTases) of Mycobacterium tuberculosis (Mtb) exhibit diversity across clinical isolates, but the forces driving this variation are not entirely clear. Recently, we observed several isolates exhibiting anomalous hypomethylation by Type I MTase Mycobacterial Adenine Methyltransferase C (MamC) despite a wild-type mamC genotype (\u2018MamC-anomalous\u2019 isolates). Investigating this hypomethylation through multiple analyses revealed three key findings. First, heterogeneity analysis revealed intercellular mosaic methylation (IMM) in MamC-anomalous isolates. While they often exhibit phase-variable heterogeneity, this is the first report of IMM by a prokaryotic Type I MTase. Second, MamC-anomalous isolates exhibited a large, stable difference in chromosome copy number along the replication axis (a proxy for bacterial growth rate), suggesting a distinct growth phase accompanied by MamC hypomethylation. Third, MamC methylation efficiency decreased progressively with distance from the origin of replication on both strands, with a marked exaggeration in MamC-anomalous isolates. In contrast, other Mtb MTases (MamA and MamB) exhibited lower methylation levels away from the origin only on the lagging strand, and without exaggeration in MamC-anomalous isolates. We conclude that, among Mtb MTases, MamC DNA methylation is uniquely linked to growth dynamics.<\/jats:p>","DOI":"10.1093\/narmme\/ugae020","type":"journal-article","created":{"date-parts":[[2024,11,16]],"date-time":"2024-11-16T03:16:10Z","timestamp":1731726970000},"source":"Crossref","is-referenced-by-count":2,"title":["Intercellular mosaic methylation in fast-growing <i>Mycobacterium tuberculosis<\/i> clinical isolates"],"prefix":"10.1093","volume":"1","author":[{"given":"Maryam","family":"Ahmadi\u00a0Jeshvaghane","sequence":"first","affiliation":[{"name":"Laboratory for Pathogenesis of Clinical Drug Resistance and Persistence, San Diego State University , San Diego , CA 92190,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samuel\u00a0J","family":"Modlin","sequence":"additional","affiliation":[{"name":"Laboratory for Pathogenesis of Clinical Drug Resistance and Persistence, San Diego State University , San Diego , CA 92190,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Derek","family":"Conkle-Gutierrez","sequence":"additional","affiliation":[{"name":"Laboratory for Pathogenesis of Clinical Drug Resistance and Persistence, San Diego State University , San Diego , CA 92190,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monica\u00a0E","family":"Espinoza","sequence":"additional","affiliation":[{"name":"Laboratory for Pathogenesis of Clinical Drug Resistance and Persistence, San Diego State University , San Diego , CA 92190,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3648-9384","authenticated-orcid":false,"given":"Faramarz","family":"Valafar","sequence":"additional","affiliation":[{"name":"Laboratory for Pathogenesis of Clinical Drug Resistance and Persistence, San Diego State University , San Diego , CA 92190,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,11,15]]},"reference":[{"key":"2025010217151378800_B1","article-title":"Global Tuberculosis Report 2022","author":"World Health Organization","year":"2022"},{"key":"2025010217151378800_B2","doi-asserted-by":"crossref","first-page":"443","DOI":"10.3389\/fcimb.2020.00443","article-title":"Investigating non-sterilizing cure in TB patients at the end of successful anti-TB therapy","volume":"10","author":"Beltran","year":"2020","journal-title":"Front. 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Microbiol."},{"key":"2025010217151378800_B45","doi-asserted-by":"crossref","first-page":"R12","DOI":"10.1186\/gb-2004-5-2-r12","article-title":"Versatile and open software for comparing large genomes","volume":"5","author":"Kurtz","year":"2004","journal-title":"Genome Biol"},{"key":"2025010217151378800_B46","doi-asserted-by":"crossref","first-page":"e0067321","DOI":"10.1128\/mSystems.00673-21","article-title":"Structure-aware Mycobacterium tuberculosis functional annotation uncloaks resistance, metabolic, and virulence genes","volume":"6","author":"Modlin","year":"2021","journal-title":"mSystems"},{"key":"2025010217151378800_B47","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1186\/s13059-019-1911-0","article-title":"SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies","volume":"20","author":"Goel","year":"2019","journal-title":"Genome Biol"},{"key":"2025010217151378800_B48","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: pairwise alignment for nucleotide sequences","volume":"34","author":"Li","year":"2018","journal-title":"Bioinformatics"},{"key":"2025010217151378800_B49","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1038\/s41592-018-0001-7","article-title":"Accurate detection of complex structural variations using single-molecule sequencing","volume":"15","author":"Sedlazeck","year":"2018","journal-title":"Nat. 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