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Genome mining and bioinformatics analyses targeting the multinuclear nonheme iron oxidative (MNIO) enzyme family led to the identification of a RiPP biosynthetic gene cluster from Streptomyces thermodiastaticus JCM 4840, the std cluster, which includes multiple biosynthetic enzymes and a precursor peptide containing a conserved SNKEWQE motif. Using in vitro approaches, we elucidated the modifications installed by the std biosynthetic enzymes. First, a YcaO-TfuA pair thioamidates the asparagine backbone. Next, a peptidase with an S8\/S53 domain fused to a NodU-like carbamoyltransferase both carbamoylates the \u03b5-amino group of lysine to produce the nonproteinogenic amino acid homocitrulline and cleaves the C-terminal EWQE motif. Finally, a partner protein-MNIO pair bis-hydroxylates the \u03b2- and \u03b3-carbon positions of the installed homocitrulline to create dihydroxyhomocitrulline. The formation of homocitrulline and dihydroxyhomocitrulline is unprecedented in RiPP biosynthesis. Moreover, these findings expand the known substrate scope of YcaO-TfuA enzymes and MNIOs and identify new roles for carbamoyltransferases in these pathways.<\/jats:p>","DOI":"10.1021\/jacs.6c09029","type":"journal-article","created":{"date-parts":[[2026,7,27]],"date-time":"2026-07-27T04:58:35Z","timestamp":1785128315000},"page":"32426-32439","source":"Crossref","is-referenced-by-count":0,"title":["Bis-hydroxylation\nof Homocitrulline Catalyzed by a\nMultinuclear Nonheme Iron Oxidative Enzyme during RiPP Biosynthesis"],"prefix":"10.1021","volume":"148","author":[{"given":"Dayna P.","family":"Hebron","sequence":"first","affiliation":[{"name":"Northwestern University , , , ,","place":["Evanston, Illinois, United States, 60208"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tucker J.","family":"Shriver","sequence":"additional","affiliation":[{"name":"Northwestern University , , , ,","place":["Chicago, Illinois, United States, 60611"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3740-9999","authenticated-orcid":true,"given":"Joshua J.","family":"Ziarek","sequence":"additional","affiliation":[{"name":"Northwestern University , , , ,","place":["Chicago, Illinois, United States, 60611"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8472-4134","authenticated-orcid":true,"given":"Amy C.","family":"Rosenzweig","sequence":"additional","affiliation":[{"name":"Northwestern University , , , ,","place":["Evanston, Illinois, United States, 60208"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,7,24]]},"reference":[{"key":"2026080511125941800_cit1","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1039\/D0NP00027B","article-title":"New Developments\nin RiPP Discovery, Enzymology and Engineering","volume":"38","author":"Montalban-Lopez","year":"2021","journal-title":"Nat. Prod. Rep."},{"key":"2026080511125941800_cit2","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1039\/C2NP20085F","article-title":"Ribosomally Synthesized and Post-Translationally\nModified Peptide Natural Products: Overview and Recommendations for\na Universal Nomenclature","volume":"30","author":"Arnison","year":"2013","journal-title":"Nat. Prod. Rep."},{"key":"2026080511125941800_cit3","doi-asserted-by":"publisher","first-page":"1838","DOI":"10.1016\/j.csbj.2020.06.032","article-title":"Genome Mining Strategies\nfor Ribosomally Synthesised\nand Post-Translationally Modified Peptides","volume":"18","author":"Russell","year":"2020","journal-title":"Comput. Struct. Biotechnol J."},{"key":"2026080511125941800_cit4","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.cbpa.2017.02.005","article-title":"Ribosomally Synthesized and Post-Translationally\nModified\nPeptide Natural Product Discovery in the Genomic Era","volume":"38","author":"Hetrick","year":"2017","journal-title":"Curr. Opin Chem. Biol."},{"key":"2026080511125941800_cit5","doi-asserted-by":"publisher","first-page":"16377","DOI":"10.1039\/D5SC90158H","article-title":"A Focus\non Unexpected Surprises in RiPP Natural Product Biosynthesis","volume":"16","author":"Thibodeaux","year":"2025","journal-title":"Chem. Sci."},{"key":"2026080511125941800_cit6","doi-asserted-by":"publisher","first-page":"102467","DOI":"10.1016\/j.cbpa.2024.102467","article-title":"Multinuclear Non-heme Iron Dependent Oxidative Enzymes\n(MNIOs) Involved in Unusual Peptide Modifications","volume":"80","author":"Chen","year":"2024","journal-title":"Curr. Opin Chem. Biol."},{"key":"2026080511125941800_cit7","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/bs.mie.2025.01.060","article-title":"Genome Mining for Natural Products Made by Multinuclear\nIron-Dependent Oxidation Enzymes (MNIOs)","volume":"717","author":"Yu","year":"2025","journal-title":"Methods\nEnzymol."},{"key":"2026080511125941800_cit8","doi-asserted-by":"publisher","first-page":"1411","DOI":"10.1126\/science.aap9437","article-title":"The Biosynthesis\nof Methanobactin","volume":"359","author":"Kenney","year":"2018","journal-title":"Science"},{"key":"2026080511125941800_cit9","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1126\/science.aau6232","article-title":"Use of\na Scaffold Peptide in the Biosynthesis of Amino\nAcid-Derived Natural Products","volume":"365","author":"Ting","year":"2019","journal-title":"Science"},{"key":"2026080511125941800_cit10","doi-asserted-by":"publisher","first-page":"1008","DOI":"10.1021\/acscentsci.3c00160","article-title":"Macrocyclization\nand Backbone Rearrangement During RiPP Biosynthesis by a SAM-Dependent\nDomain-of-Unknown-Function 692","volume":"9","author":"Ayikpoe","year":"2023","journal-title":"ACS Cent. 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Biol."},{"key":"2026080511125941800_cit32","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1021\/acschembio.8b01058","article-title":"Salinipeptins:\nIntegrated Genomic and Chemical Approaches Reveal Unusual d-Amino\nAcid-Containing Ribosomally Synthesized and Post-Translationally Modified\nPeptides (RiPPs) from a Great Salt Lake Streptomyces sp","volume":"14","author":"Shang","year":"2019","journal-title":"ACS Chem. Biol."},{"key":"2026080511125941800_cit33","doi-asserted-by":"publisher","first-page":"6135","DOI":"10.1038\/s41467-022-33890-w","article-title":"A Scalable Platform\nto Discover Antimicrobials\nof Ribosomal Origin","volume":"13","author":"Ayikpoe","year":"2022","journal-title":"Nat. Commun."},{"key":"2026080511125941800_cit34","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2123566119","article-title":"A Mixed-valent\nFe(II)Fe(III) Species\nConverts Cysteine to an Oxazolone\/Thioamide Pair in Methanobactin\nBiosynthesis","volume":"119","author":"Park","year":"2022","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2026080511125941800_cit35","doi-asserted-by":"publisher","first-page":"302","DOI":"10.1038\/s41422-022-00620-2","article-title":"Crystal structure\nand catalytic mechanism of the MbnBC holoenzyme required for methanobactin\nbiosynthesis","volume":"32","author":"Dou","year":"2022","journal-title":"Cell Res."},{"key":"2026080511125941800_cit36","doi-asserted-by":"publisher","first-page":"6617","DOI":"10.1038\/s41467-022-34387-2","article-title":"Endowing Homodimeric\nCarbamoyltransferase GdmN with Iterative Functions\nThrough Structural Characterization and Mechanistic Studies","volume":"13","author":"Wei","year":"2022","journal-title":"Nat. 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Prod."},{"key":"2026080511125941800_cit47","doi-asserted-by":"publisher","first-page":"10749","DOI":"10.1021\/jacs.8b04238","article-title":"Biosynthesis\nof the Thiopeptins and\nIdentification of an F420H2-Dependent Dehydropiperidine\nReductase","volume":"140","author":"Ichikawa","year":"2018","journal-title":"J. Am. Chem. Soc."},{"key":"2026080511125941800_cit48","doi-asserted-by":"publisher","first-page":"16472","DOI":"10.1002\/anie.202102571","article-title":"Nocathioamides, Uncovered\nby a Tunable Metabologenomic Approach, Define a Novel Class of Chimeric\nLanthipeptides","volume":"60","author":"Saad","year":"2021","journal-title":"Angew. Chem., Int. Ed. Engl."},{"key":"2026080511125941800_cit49","doi-asserted-by":"publisher","first-page":"4046","DOI":"10.1002\/anie.201108896","article-title":"The O-carbamoyltransferase\nTobZ Catalyzes an Ancient Enzymatic Reaction","volume":"51","author":"Parthier","year":"2012","journal-title":"Angew. Chem., Int. Ed. 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