DOI: 10.1073/pnas.2615454123 ISSN: 0027-8424
Biosynthetic origin of anticancer dolastatin 15 reveals a noncanonical NRPS architecture enabling 2-keto acid activation
Manyun Chen, Jie Liu, Hsin-Ying Tsai, Cheng-Yu Li, Jeremiah D. Batucan, Campbell W. Eckhardt, Tam H. D. Pham, Emma K. Ellis, Ranjala Ratnayake, Valerie J. Paul, Steven D. Bruner, Mohamed S. Donia, Hendrik Luesch, Yousong Ding
Elucidating the biological origins and biosynthetic pathways of marine natural products remains a major challenge, particularly for compounds derived from microbial consortia. Here, we identify the marine cyanobacterial genus
Dapis
as the source of the potent anticancer natural product dolastatin 15 using genome-resolved metagenomics. Reconstruction of two complete and two near-complete genomes provides genome-resolved characterization of the genus
Dapis
, revealing extensive biosynthetic potential. Genome mining identified the dolastatin 15 biosynthetic gene cluster. Subsequent analyses reconstructed its pathway and uncovered a noncanonical five-domain nonribosomal peptide synthetase module containing an embedded 2-keto acid–activating domain, revealing an unexpected architectural solution for incorporating 2-keto acid-derived hydroxy acid building blocks. Comparative and evolutionary analyses support a model in which this architecture may have arisen through recruitment of keto acid-activating domains and reduction of canonical adenylation domain features. We further biochemically and structurally characterize an
O
-methyltransferase that catalyzes formation of the characteristic methoxy pyrrolinone moiety, thereby validating a key terminal tailoring step in the proposed biosynthetic pathway. Together, these findings define the biosynthetic logic of dolastatin 15 and expand understanding of substrate activation and assembly-line diversification in nonribosomal peptide biosynthesis.