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New lectins from Codium isthmocladum Vickers show unique amino acid sequence and antibiofilm effect on pathogenic bacteria

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Abstract

Two new lectins from the green alga Codium isthmocladum (CiL-1 and CiL-2) were isolated. Both lectins could agglutinate human and rabbit erythrocytes. Galactosides and fetuin showed inhibitory effect on CiL-1. CiL-2 was inhibited by GalNAc and porcine stomach mucin. CiL-1 was a monomeric protein of 12 kDa, whereas CiL-2 showed 12 kDa in SDS-PAGE and an oligomeric state in gel filtration. MALDI-ToF-MS of CiL-1 revealed a molecular mass of 12.027 ± 5 Da, while CiL-2 showed molecular mass of 12.264 ± 5 Da. Ninety-eight percent of CiL-1’s primary structure was determined consisting of 112 residues placed in two repeated domains with approximately 60% of similarity. CiL-1 showed similarity with hypothetical proteins from aquatic pathogenic fungi. The N-terminal of CiL-2 showed no similarity to CiL-1 or to any known protein. The three-dimensional model of CiL-1 consists of four two-strand β-sheets disposed in a barrel-like arrangement, connected by loops of variable sizes, with a well-structured hydrophobic core. Binding site prediction suggests the existence of two independent monosaccharide binding sites in CiL-1. The lectins showed no antibacterial activity on Gram-positive and Gram-negative bacteria, but they were able to significantly inhibit the biofilm formation from Staphylococcus aureus and Staphylococcus epidermidis.

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Acknowledgments

The authors would like to acknowledge the Centro de Tecnologias Estratégicas do Nordeste (CETENE) for providing equipment and technical support for experiments involving MALDI-ToF. The authors are grateful to Professor David Martin for helping in the English writing. A.H.S., and E.H.T. are senior investigators of CNPq. The authors dedicate this article to the memory of Professor David J. Rogers.

Funding

This work was supported by the Brazilian agencies CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), FUNCAP (Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico), and FINEP (Financiadora de Estudos e Projetos).

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Authors and Affiliations

  1. Laboratório de Biotecnologia Marinha - BioMar-Lab, Departamento de Engenharia de Pesca, Universidade Federal do Ceará, Campus do Pici s/n, bloco 871, Av. Mister Hull, Box 6043, Fortaleza, Ceará, 60440-970, Brazil

    Rômulo Farias Carneiro, Philippe Lima Duarte, Renata Pinheiro Chaves, Ramon Rodrigues Feitosa, Alexandre Holanda Sampaio & Celso Shiniti Nagano

  2. Campus Monte Alegre, Universidade do Oeste do Pará, Av. Major Francisco Mariano s/n - Bairro Cidade Alta, Monte Alegre, PA, 68220-000, Brazil

    Suzete Roberta da Silva

  3. Faculdade de Filosofia Dom Aureliano Matos, Universidade Estadual do Ceará, Av. Dom Aureliano Matos, 2060, Limoeiro do Norte, CE, 62930-000, Brazil

    Bruno Lopes de Sousa

  4. Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Campus do Pici s/n, bloco 871, Fortaleza, Ceará, 60440-970, Brazil

    Antônio Willame da Silva Alves & Bruno Anderson Matias da Rocha

  5. Departamento de Ciências Biológicas, Faculdade de Ciências Exatas e Naturais, Universidade do Estado do Rio Grande do Norte, Mossoró, Rio Grande do Norte, 59625-620, Brazil

    Mayron Alves de Vasconcelos

  6. Laboratório Integrado de Biomoléculas - LIBS, Departamento de Patologia e Medicina Legal, Universidade Federal do Ceará, Monsenhor Furtado, s/n, Fortaleza, Ceará, 60430-160, Brazil

    Mayron Alves de Vasconcelos & Edson Holanda Teixeira

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  1. Rômulo Farias Carneiro
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Supplementary Figure 1.

Determination of cysteine pairing by ESI-MS/MS. A) Mass spectra of the ion at m/z 670.26. B) Mass spectra of the ion at m/z 708.93. C) Mass spectra of the ion at m/z 878.33. D) Mass spectra of the ion at m/z 936.33. (PNG 251 kb)

High resolution image (TIF 273 kb)

Supplementary Figure 2.

CD spectra of C. isthmocladum lectins. (A) Far-UV CD spectra of CiL-1 (190-240 nm). (B) Far-UV CD spectra of CiL-2 (190-240 nm). (PNG 110 kb)

High resolution image (TIF 126 kb)

Supplementary Figure 3.

Ramachandran plot for CiL-1 structural model. (PNG 14 kb)

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(DOCX 17 kb)

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Carneiro, R.F., Duarte, P.L., Chaves, R.P. et al. New lectins from Codium isthmocladum Vickers show unique amino acid sequence and antibiofilm effect on pathogenic bacteria. J Appl Phycol 32, 4263–4276 (2020). https://doi.org/10.1007/s10811-020-02198-x

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