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A distinctive family of L,D-transpeptidases catalyzing L-Ala-mDAP crosslinks in Alpha- and Betaproteobacteria
Umeå University, Faculty of Medicine, Molecular Infection Medicine Sweden (MIMS). Umeå University, Faculty of Medicine, Umeå Centre for Microbial Research (UCMR). Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine). Chr. Hansen A/S, Microbial Physiology, R & amp;D, Hoersholm, Denmark.
Umeå University, Faculty of Medicine, Molecular Infection Medicine Sweden (MIMS). Umeå University, Faculty of Medicine, Umeå Centre for Microbial Research (UCMR). Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine).ORCID iD: 0000-0003-2429-7542
Umeå University, Faculty of Medicine, Molecular Infection Medicine Sweden (MIMS). Umeå University, Faculty of Medicine, Umeå Centre for Microbial Research (UCMR). Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine).ORCID iD: 0000-0002-0450-1430
Umeå University, Faculty of Medicine, Department of Medical Biochemistry and Biophysics. Umeå University, Faculty of Medicine, Wallenberg Centre for Molecular Medicine at Umeå University (WCMM).ORCID iD: 0000-0003-4165-9277
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2024 (English)In: Nature Communications, E-ISSN 2041-1723, Vol. 15, no 1, article id 1343Article in journal (Refereed) Published
Abstract [en]

The bacterial cell-wall peptidoglycan is made of glycan strands crosslinked by short peptide stems. Crosslinks are catalyzed by DD-transpeptidases (4,3-crosslinks) and LD-transpeptidases (3,3-crosslinks). However, recent research on non-model species has revealed novel crosslink types, suggesting the existence of uncharacterized enzymes. Here, we identify an LD-transpeptidase, LDTGo, that generates 1,3-crosslinks in the acetic-acid bacterium Gluconobacter oxydans. LDTGo-like proteins are found in Alpha- and Betaproteobacteria lacking LD3,3-transpeptidases. In contrast with the strict specificity of typical LD- and DD-transpeptidases, LDTGo can use non-terminal amino acid moieties for crosslinking. A high-resolution crystal structure of LDTGo reveals unique features when compared to LD3,3-transpeptidases, including a proline-rich region that appears to limit substrate access, and a cavity accommodating both glycan chain and peptide stem from donor muropeptides. Finally, we show that DD-crosslink turnover is involved in supplying the necessary substrate for LD1,3-transpeptidation. This phenomenon underscores the interplay between distinct crosslinking mechanisms in maintaining cell wall integrity in G. oxydans.

Place, publisher, year, edition, pages
Springer Nature, 2024. Vol. 15, no 1, article id 1343
National Category
Biochemistry and Molecular Biology
Identifiers
URN: urn:nbn:se:umu:diva-221654DOI: 10.1038/s41467-024-45620-5PubMedID: 38351082Scopus ID: 2-s2.0-85185130975OAI: oai:DiVA.org:umu-221654DiVA, id: diva2:1842313
Funder
Swedish Research Council, 2018- 02823Swedish Research Council, 2018-05882The Kempe Foundations, SMK2062Knut and Alice Wallenberg FoundationSwedish Research Council, 2018-07152Swedish Research Council, 2016-03599Swedish Research Council Formas, 2019- 02496The Kempe Foundations, SMK-1762The Kempe Foundations, SMK-1869Available from: 2024-03-04 Created: 2024-03-04 Last updated: 2024-07-12Bibliographically approved

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Espaillat, AkbarAlvarez, LauraTorrens, Gabrielter Beek, JosyIrazoki, OihaneBerntsson, Ronnie P-A.Cava, Felipe

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Espaillat, AkbarAlvarez, LauraTorrens, Gabrielter Beek, JosyIrazoki, OihaneBerntsson, Ronnie P-A.Cava, Felipe
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Molecular Infection Medicine Sweden (MIMS)Umeå Centre for Microbial Research (UCMR)Department of Molecular Biology (Faculty of Medicine)Department of Medical Biochemistry and BiophysicsWallenberg Centre for Molecular Medicine at Umeå University (WCMM)
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