Structural basis of cell wall anchoring by SLH domains in Paenibacillus alvei

• Published in: Nature communications 2018-08, Vol.9 (1), p.3120-11, Article 3120
• Main Authors: Blackler, Ryan J., López-Guzmán, Arturo, Hager, Fiona F., Janesch, Bettina, Martinz, Gudrun, Gagnon, Susannah M. L., Haji-Ghassemi, Omid, Kosma, Paul, Messner, Paul, Schäffer, Christina, Evans, Stephen V.
• Format: Article
• Language: English
• Subjects: 631/326/41/2536; 631/45/221; 631/45/535/1266; Amino Acid Motifs; Anchoring; Bacillus anthracis; Bacteria; Binding; Cell Proliferation; Cell Wall - chemistry; Circular Dichroism; Crystal structure; Crystallization; Domain walls; Gram-positive bacteria; Homology; Humanities and Social Sciences; Ligands; multidisciplinary; Mutagenesis; Mutagenesis, Site-Directed; Paenibacillus - cytology; Paenibacillus alvei; Peptidoglycan - chemistry; Peptidoglycans; Polymers; Prokaryotes; Protein Binding; Protein Domains; Proteins; Recombinant Proteins - chemistry; Science; Science (multidisciplinary); Trimers; Virulence
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-018-05471-3

Self-assembling protein surface (S-) layers are common cell envelope structures of prokaryotes and have critical roles from structural maintenance to virulence. S-layers of Gram-positive bacteria are often attached through the interaction of S-layer homology (SLH) domain trimers with peptidoglycan-linked secondary cell wall polymers (SCWPs). Here we present an in-depth characterization of this interaction, with co-crystal structures of the three consecutive SLH domains from the Paenibacillus alvei S-layer protein SpaA with defined SCWP ligands. The most highly conserved SLH domain residue SLH-Gly29 is shown to enable a peptide backbone flip essential for SCWP binding in both biophysical and cellular experiments. Furthermore, we find that a significant domain movement mediates binding by two different sites in the SLH domain trimer, which may allow anchoring readjustment to relieve S-layer strain caused by cell growth and division. Gram-positive bacterial envelopes comprise proteinaceous surface layers (S-layers) important for survival and virulence that are often anchored to the cell wall through secondary cell wall polymers. Here the authors use a structural and biophysical approach to define the molecular mechanism of this important interaction.