Biosynthesis of 3-thia-α-amino acids on a carrier peptide

Proc Natl Acad Sci U S A. 2022 Jul 19;119(29):e2205285119. doi: 10.1073/pnas.2205285119. Epub 2022 Jul 5.

Abstract

A subset of natural products, such as polyketides and nonribosomal peptides, is biosynthesized while tethered to a carrier peptide via a thioester linkage. Recently, we reported that the biosyntheses of 3-thiaglutamate and ammosamide, single amino acid-derived natural products, employ a very different type of carrier peptide to which the biosynthetic intermediates are bound via an amide linkage. During their biosyntheses, a peptide aminoacyl-transfer ribonucleic acid (tRNA) ligase (PEARL) first loads an amino acid to the C terminus of the carrier peptide for subsequent modification by other enzymes. Proteolytic removal of the modified C-terminal amino acid yields the mature product. We termed natural products that are biosynthesized using such pathways pearlins. To investigate the diversity of pearlins, in this study we experimentally characterized another PEARL-encoding biosynthetic gene cluster (BGC) from Tistrella mobilis (tmo). The enzymes encoded in the tmo BGC transformed cysteine into 3-thiahomoleucine both in vitro and in Escherichia coli. During this process, a cobalamin-dependent radical S-adenosylmethionine (SAM) enzyme catalyzes C-isopropylation. This work illustrates that the biosynthesis of amino acid-derived natural products on a carrier peptide is a widespread strategy in nature and expands the spectrum of thiahemiaminal analogs of amino acids that may serve a broader, currently unknown function.

Keywords: 3-thiahomoleucine; RiPP; carrier protein; pearlin; radical SAM methyltransferase.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / chemistry
  • Biological Products*
  • Escherichia coli / genetics
  • Peptide Biosynthesis, Nucleic Acid-Independent*
  • Peptide Synthases / genetics
  • Peptides
  • Polyketides*
  • Rhodospirillaceae
  • S-Adenosylmethionine

Substances

  • Amino Acids
  • Biological Products
  • Peptide Synthases
  • Peptides
  • Polyketides
  • S-Adenosylmethionine

Supplementary concepts

  • Tistrella mobilis