TRNA Involvement in Peptidoglycan Synthesis: the Work of Dieter Söll

Abstract

Biosynthesis of the Peptidoglycan of Bacterial Cell Walls. VI. Incorporation of l-Threonine into Interpeptide Bridges in Micrococcus roseus (Roberts, W. S. L., Strominger, J. L., and Söll, D. (1968) J. Biol. Chem. 243, 749–756) Biosynthesis of the Peptidoglycan of Bacterial Cell Walls. VII. Incorporation of Serine and Glycine into Interpeptide Bridges in Staphylococcus epidermidis (Petit, J.-F., Strominger, J. L., and Söll, D. (1968) J. Biol. Chem. 243, 757–767) Biosynthesis of the Peptidoglycan of Bacterial Cell Walls. X. Further Study of the Glycyl Transfer Ribonucleic Acids Active in Peptidoglycan Synthesis in Staphylococcus aureus (Bumsted, R. M., Dahl, J. L., Söll, D., and Strominger, J. L. (1968) J. Biol. Chem. 243, 779–782) Dieter Söll was born in 1935. He earned his Ph.D. from Stuttgart University in 1962, after which he did a postdoctoral fellowship at the University of Wisconsin, Madison. He then joined the faculty of the University of Wisconsin and was an assistant professor there until 1967, when he joined the faculty of Yale University. Söll remains at Yale today as Sterling Professor of Molecular Biophysics and Biochemistry and Professor of Chemistry. While at the University of Wisconsin, Söll published several papers with Jack Strominger, who will be the subject of a future Journal of Biological Chemistry (JBC) Classic. In the papers, Söll and Strominger identified several tRNAs that participate in peptidoglycan formation. This was an exciting discovery as aminoacyl-tRNA was only thought to be involved in ribosome-catalyzed protein synthesis. Peptidoglycan is a polymer of sugars and amino acids that forms a homogeneous layer outside the plasma membrane of eubacteria. It serves a structural role in the bacterial cell wall, giving it shape and strength, as well as counteracting the osmotic pressure of the cytoplasm. The peptidoglycan layer is a crystal lattice formed by linear chains of N-acetylglucosamine and N-acetylmuramic acid that are connected by short (4–5-residue) amino acid chains. The nature of the bridge is to some extent genus-specific. In the first JBC Classic reprinted here, Söll, Strominger, and W. S. L. Roberts investigate the biosynthesis of peptidoglycan in Micrococcus roseus. It had previously been shown that in the formation of the Staphylococcus aureus pentaglycine peptidoglycan cross-bridge, glycine is activated, attached to tRNA, and then transferred from glycyl-tRNA to a lipid intermediate, which is utilized to form the peptidoglycan. Söll, Strominger, and Roberts isolated two threonyl-tRNAs from M. roseus R27 which catalyzed the incorporation of l-threonine onto the ϵ-amino group of lysine in the bacteria's interpeptide bridge. The threnyl-tRNAs were also able to catalyze protein biosynthesis. The second JBC Classic, which appeared back-to-back with the first paper, reports on the tRNA-dependent incorporation of serine in the interpeptide bridge of S. epidermidis. Söll, Strominger, and J.-F. Petit isolated four seryl-tRNAs involved in the transfer of serine to a lipid intermediate of peptidoglycan synthesis. However, only three of the tRNAs could be shown to participate in protein synthesis. Söll proposed several possibilities for the fourth tRNA (Ser IIA) including that “Ser IIA is a form of suppressor tRNA. That is, it would respond in protein synthesis, but to a coding triplet other than a normal serine triplet.” It was later discovered that this was indeed the bacterial selenocysteine tRNA. Twenty years later, Söll was the first to sequence the Escherichia coli selenocysteine tRNA (1Schön A. Bock A. Ott G. Sprinzl M. Söll D. The selenocysteine-inserting opal suppressor serine tRNA from E. coli is highly unusual in structure and modification.Nucleic Acids Res. 1989; 17: 7159-7165Crossref PubMed Scopus (67) Google Scholar). In the final JBC Classic, Söll, Strominger, R. M. Bumsted, and J. L. Dahl report on their isolation of three glycine acceptor tRNAs from S. aureus. All three tRNAs were active in peptidoglycan synthesis, but only two could produce polypeptides. Söll has received several awards and honors for his research, including the 1988 Alexander von Humbolt U. S. Senior Scientist Award. He is a Fellow of the American Association of the Advancement of Science and the American Academy of Microbiology and is a member of the National Academy of Sciences.