Structural insights and antimicrobial synergy of a proto-galectin from the marine sponge Aiolochroia crassa

• Published in: Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2025-01, Vol.275, p.111034, Article 111034
• Main Authors: Torres, Renato Cezar Farias, Júnior, Israel Ferreira Barbosa, Souza, Victoria Régia Pinto de, Duarte, Jéssica de Assis, Chaves, Renata Pinheiro, Costa Filho, Manoel Ferreira da, Nascimento, Elielton, Malveira, Ellen Araujo, Andrade, Alexandre Lopes, Pinheiro, Ulisses, Vasconcelos, Mayron Alves de, de Sousa, Bruno Lopes, Teixeira, Edson Holanda, Carneiro, Rômulo Farias, Nagano, Celso Shiniti, Sampaio, Alexandre Holanda
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; amino acids; Animals; Anti-Bacterial Agents - chemistry; Anti-Bacterial Agents - pharmacology; Antibiotics; biofilm; Biofilms - drug effects; Biofilms - growth & development; carbohydrate binding; cattle; Drug Synergism; electron microscopy; Escherichia coli; Escherichia coli - drug effects; fetuins; Galectin; galectins; Galectins - chemistry; Galectins - isolation & purification; Galectins - metabolism; Galectins - pharmacology; Marine sponge; mass spectrometry; Molecular Docking Simulation; mucins; polysaccharides; Porifera; Porifera - chemistry; sialic acid; Staphylococcus aureus; Staphylococcus aureus - drug effects; Staphylococcus epidermidis
• ISSN: 1096-4959; 1879-1107; 1879-1107
• DOI: 10.1016/j.cbpb.2024.111034

In this study, we isolated a novel lectin from the marine sponge Aiolochroia crassa, named AcrL. The lectin showed a preference for glycans containing sialic acid terminal residues, as indicated by the strongest inhibition with fetuin and bovine submaxillary mucin. Primary structure determination by mass spectrometry revealed that AcrL is a galectin with conserved amino acid residues typically involved in carbohydrate binding. Structural modeling indicated that AcrL adopts a typical galectin β-sandwich motif, featuring two anti-parallel β-sheets with five strands each. Docking calculations revealed a carbohydrate-binding site composed of a main site, capable of hosting galactopyranosides, and an extended site, facilitating the binding of complex carbohydrates. AcrL inhibited significant biofilm formation against Staphylococcus aureus, S. epidermidis, and Escherichia coli with concentrations ranging from 500 to 15.6 μg.mL−1 for S. aureus, 7.8 μg.mL−1 for S. epidermidis, and 500 μg.mL−1 for E. coli. Furthermore, when combined with different antibiotics, AcrL potentiated their effect against pathogenic bacteria. The antimicrobial mechanism of AcrL was investigated using scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM). The analysis indicates that AcrL induces damage to the bacterial membrane. These findings underscore the discovery of a novel galectin in a basal organism and the comprehensive biochemical characterization conducted in this research, highlighting the potential of AcrL as a novel antibacterial agent and emphasizing its importance in combating bacterial infections. [Display omitted] •Discovery of a novel galectin, AcrL, from the marine sponge Aiolochroia crassa•AcrL exhibits strong binding to sialic acid-containing glycans.•Structural modeling reveals AcrL adopts a typical galectin β-sandwich motif.•AcrL effectively inhibits biofilm formation of various pathogenic bacteria.•AcrL potentiates the effects of antibiotics against bacterial infections.