Genomic elements associated with biofilm formation in Lactobacillus delbrueckii subspecies bul-garicus and Lactobacillus delbrueckii subspecies lactis
DOI:
https://doi.org/10.18633/biotecnia.v26.2423Keywords:
pili gene, srtA gene, inu gene, epsD gene, bioinformaticAbstract
Lactobacillus delbrueckii subsp. bulgaricus and L. delbrueckii subsp. lactis are two biotechnologically important subspecies within the group of lactic acid bacteria. Both are used to obtain products based on lactic fermentation and their activity as probiotics has been reported. The aim of the present study was to identify and compare the genomic elements associated with biofilm formation in both subspecies using computational tools. The bibliometric analysis showed that adhesin genes, exopolysaccharide synthesis genes, and cis- and trans-regulatory elements could be associated with biofilm formation in both subspecies. The comparison of 12 genomes of L. delbrueckii subsp. bulgaricus and 7 of L. delbrueckii subsp. lactis detected the presence of the pili and srtA genes in a conserved operon with identity percentages greater than 97 % between both subspecies. The inu gene that has a levansucrase function was also identified. Finally, the epsD gene was found, present in a polycistronic transcriptional unit, encoding an enzyme associated with the synthesis of heteropolysaccharides. These data show, by first time, evidence of the presence of genes that participate in biofilm formation in L. delbrueckii subsp. bulgaricus and L. delbrueckii subsp. lactis strains.
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Alkema, W.B.L., Lenhard, B., Wasserman, W.W. 2004. Regulog analysis: Detection of conserved regulatory networks across bacteria: Application to Staphylococcus aureus. Genome Res. 7:1362-73.
Altschup, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J. 1990. Basic Local Alignment Search Tool. J. Mol. Biol. Vol. 215.
Baek, M.G., Kim, K.W., Yi, H. 2023. Subspecies-level genome comparison of Lactobacillus delbrueckii. Sci Rep. 13(1).
Caggianiello, G., Kleerebezem, M., Spano, G. 2016. Exopolysaccharides produced by lactic acid bacteria: from health-promoting benefits to stress tolerance mechanisms. Applied Microbiology and Biotechnology. 100:3877-86.
Chen, C., Zhao, G., Chen, W., Guo, B. 2015. Metabolism of fructooligosaccharides in Lactobacillus plantarum ST-III via differential gene transcription and alteration of cell membrane fluidity. Appl Environ Microbiol. 81(22):7697-707.
Sarduy Bermúdez L, González Díaz M.E., La biopelícula: una nueva concepción de la placa dentobacteriana Biofilm: a new conception of dentobacterial plaque. Medicentro electronica.Vol. 20. 2016.
Cuadros-Orellana, S., Martin-Cuadrado, A.B., Legault, B., D’Auria, G., Zhaxybayeva, O., Papke, R.T., Rodriguez-Valera, F. 2007. Genomic plasticity in prokaryotes: The case of the square haloarchaeon. ISME Journal. 1(3):235-45.
De Angelis, M., Gobbetti, M. 2004. Environmental stress responses in Lactobacillus: A review. Proteomics. 4:106-22.
De Angelis, M., Siragusa, S., Campanella, D., Di Cagno, R., Gobbetti, M. 2015. Comparative proteomic analysis of biofilm and planktonic cells of Lactobacillus plantarum DB200. Proteomics. 15(13):2244-57.
de Crécy-Lagard, V., El Yacoubi, B., de la Garza, R.D., Noiriel, A., Hanson, A.D. 2007. Comparative genomics of bacterial and plant folate synthesis and salvage: Predictions and validations. BMC Genomics. 23;8.
De Jesus, L.C.L., Aburjaile, F.F., Sousa, T.D.J., Felice, A.G., Soares, S.D.C., Alcantara, L.C.J., De Carvalho, A.V.A. 2022. Genomic Characterization of Lactobacillus delbrueckii Strains with Probiotics Properties. Frontiers in Bioinformatics. 6;2.
De Jesus, L.C.L., Drumond, M.M., de Carvalho, A., Santos, S.S., Martins, F.S., Ferreira, Ê., Salgado, F.R., Do Carmo, F.L., Perez, P.F., Carvalho, A., Vascos, A., Mancha, A.P. 2019. Protective effect of Lactobacillus delbrueckii subsp. lactis CIDCA 133 in a model of 5 Fluorouracil-Induced intestinal mucositis. J Funct Foods. 53:197-207.
Defrance, M., Janky, R., Sand, O., van Helden, J. 2008. Using RSAT oligo-analysis and dyad-analysis tools to discover regulatory signals in nucleic sequences. Nat Protoc. 3(10):1589-603.
El-Sayed, A., Aleya, L., & Kamel, M. 2021. Microbiota's role in health and diseases. Environmental science and pollution research international, 28(28), 36967–36983.
Frazer, K.A., Pachter, L., Poliakov, A., Rubin, E.M., Dubchak, I. 2004. VISTA: Computational tools for comparative genomics. Nucleic Acids Res. 1;32(WEB SERVER ISS.).
Giltner, C.L., Nguyen, Y., Burrows, L.L. 2012. Type IV Pilin Proteins: Versatile Molecular Modules. Microbiology and Molecular Biology Reviews. 76(4):740-72.
Guiton, P.S., Hung, C.S., Kline, K.A., Roth, R., Kau, A.L., Hayes, E., Heuser., Dodson, K.W., Caparon, M.G., Hultgren, S.J. 2009. Contribution of autolysin and sortase A during Enterococcus faecalis DNA-dependent biofilm development. Infect Immun. 77(9):3626-38.
Hao, P., Zheng, H., Yu, Y., Ding, G., Gu, W., Chen, S., Zhonghao, Y, Munehiro, O., Tomonobu, K., Shengyue, W., Xuan, L., Zai-Si, J., Guoping, Z. 2011. Complete sequencing and pan-genomic analysis of Lactobacillus delbrueckii subsp. bulgaricus reveal its genetic basis for industrial yogurt production. PLoS One. 6(1).
Jones, S.E., Versalovic, J. 2009. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol. 9.
Lamothe, G., Jolly, L., Mollet, B., Stingele, F. 2002. Genetic and biochemical characterization of exopolysaccharide biosynthesis by Lactobacillus delbrueckii subsp. bulgaricus. Arch Microbiol. 178(3):218-28.
Laurenceau, R., Péhau-Arnaudet, G., Baconnais, S., Gault, J., Malosse, C., Dujeancourt, A., Campo, N., Chamot-Rooke, J., Le EL., Claverys, J.P., Fronzes, R. 2013. A Type IV Pilus Mediates DNA Binding during Natural Transformation in Streptococcus pneumoniae. PLoS Pathog. 9(6).
Lebeer, S., Claes, I., Tytgat, H.L.P., Verhoeven, T.L.A., Marien, E., von Ossowski, I., Reunanen, J., Palva, A., De Vos, W.M., De Keersmaecker, S.C.J., Vanderleyden, J. 2012. Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl Environ Microbiol. 78(1):185-93.
Lebeer, S., De Keersmaecker, S.C.J., Verhoeven, T.L.A., Fadda, A.A., Marchal, K., Vanderleyden, J. 2007. Functional analysis of luxS in the probiotic strain Lactobacillus rhamnosus GG reveals a central metabolic role important for growth and biofilm formation. J Bacteriol. 189(3):860-71.
Lebeer, S., Verhoeven, T.L.A., Francius, G., Schoofs, G., Lambrichts, I., Dufrêne, Y., Vanderleyden, J., De Keersmaecker, S.C.J. 2009. Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl Environ Microbiol. 75(11):3554-63.
Malik, S., Petrova, M.I., Claes, I.J.J., Verhoeven, T.L.A., Busschaert, P., Vaneechoutte, M., Lievens, Bart., Lambrichts, I., Sienzen, R.J., Balzarini, J., Vanderleyden., Lebeer, S. 2013. The highly autoaggregative and adhesive phenotype of the vaginal Lactobacillus plantarum strain cmpg5300 is sortase dependent. Appl Environ Microbiol. 79(15):4576-85.
Million, M., Maraninchi, M., Henry, M., Armougom, F., Richet, H., Carrieri, P., Valero, R., Raccah, D., Vialettes, B., Raoult, D. 2012. Obesity-associated gut microbiota is enriched in Lactobacillus reuteri and depleted in Bifidobacterium animalis and Methanobrevibacter smithii. Int J Obes. 36(6):817-25.
Muscariello, L., Marino, C., Capri, U., Vastano, V., Marasco, R., Sacco, M. 2013. CcpA and three newly identified proteins are involved in biofilm development in Lactobacillus plantarum. J Basic Microbiol. 53(1):62-71.
Newman, J.A., Rodrigues, C., Lewis, R.J. 2013. Molecular basis of the activity of SinR Protein, the master regulator of biofilm formation in Bacillus subtilis. Journal of Biological Chemistry. 12;288(15):10766-78.
Oxaran, V., Ledue-Clier, F., Dieye, Y., Herry, J.M., Péchoux, C., Meylheuc, T., Briandet, R., Juillard, V., Piard, J.C. 2012. Pilus Biogenesis in Lactococcus lactis: Molecular Characterization and Role in Aggregation and Biofilm Formation. PLoS One. 6;7(12).
Oyeniran, A., Gyawali, R., Aljaloud, S.O., Krastanov, A., Ibrahim, S.A. 2020. Probiotic Characteristics and Health Benefits of the Yogurt Bacterium Lactobacillus delbrueckii sp. bulgaricus. Available from: http://dx.doi.org/10.5772/intechopen.86939
Pessione, E. 2012. Lactic acid bacteria contribution to gut microbiota complexity: lights and shadows. Frontiers in cellular and infection microbiology. 2:86.
Rizzello, C.G., De Angelis, M. 2011. Lactic Acid Bacteria Lactobacillus spp.: Lactobacillus delbrueckii Group. Encyclopedia of Dairy Sciences: Second Edition. 1;119-24.
Ronish, L.A., Lillehoj, E., Fields, J.K., Sundberg, E.J., Piepenbrink, K.H. 2019. The structure of PilA from Acinetobacter baumannii AB5075 suggests a mechanism for functional specialization in Acinetobacter type IV pili. Journal of Biological Chemistry. 4;294(1):218-30.
Ruas-Madiedo, P.2009. Biosynthesis and Chemical Composition of Exopolysaccharides Produced by Lactic Acid Bacteria. Bacterial polysaccharides: current innovations and future trends. p. 279-310.
Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Ad` Rajandream, M.A., Barrell, B. 2000. Artemis: sequence visualization and annotation [Internet]. Vol. 16, BIOINFORMATICS APPLICATIONS NOTE. Available from: http://www.acedb.org/
Sadekuzzaman, M., Yang, S., Mizan, M.F.R., Ha, S.D. 2015. Current and Recent Advanced Strategies for Combating Biofilms. Compr Rev Food Sci Food Saf. 14(4):491-509.
Santana-Garcia, W., Castro-Mondragon, J.A., Padilla-Gálvez, M., Nguyen, N.T.T., Elizondo-Salas, A., Ksouri, N., Gerbes, F., Thieffry, D., Vincens, P., Contrras-Moreira, B., Helden, J.V., Thomas-Chollier, M., Medina-Rivera, A. 2022. RSAT 2022: regulatory sequence analysis tools. Nucleic Acids Res. 5;50(W1): W670-6.
Schwab, C., Walter, J., Tannock, G.W., Vogel, R.F., Gänzle, M.G. 2007. Sucrose utilization and impact of sucrose on glycosyltransferase expression in Lactobacillus reuteri. Syst Appl Microbiol. 10;30(6):433-43.
Sheppard, D., Berry, J.L., Denise, R., Rocha, E.P.C., Matthews, S. 2020. Pelicic V. The major subunit of widespread competence pili exhibits a novel and conserved type IV pilin fold. Journal of Biological Chemistry. 8;295(19):6594-604.
Suzzi, G., Sidari, R., Reinheimer, J., Liu, F., Huo, G., Evivie, S.E. 2020. Lactobacillus delbrueckii subsp. bulgaricus KLDS 1.0207 Exerts Antimicrobial and Cytotoxic Effects in vitro and Improves Blood Biochemical Parameters in vivo Against Notable Foodborne Pathogens.; Available from: www.frontiersin.org
Taboada, B., Estrada, K., Ciria, R., Merino, E. 2018. Operon-mapper: A web server for precise operon identification in bacterial and archaeal genomes. Bioinformatics. 1;34(23):4118-20.
Tieking, M., Gänzle, M.G. 2005. Exopolysaccharides from cereal-associated Lactobacilli. In: Trends in Food Science and Technology. 79-84.
Walter, J., Schwab, C., Loach, D.M., Gänzle, M.G., Tannock, G.W. 2008. Glucosyltransferase A (GtfA) and inulosucrase (Inu) of Lactobacillus reuteri TMW1.106 contribute to cell aggregation, in vitro biofilm formation, and colonization of the mouse gastrointestinal tract. Microbiology. 154(1):72-80.
Wen, Z.T., Baker, H.V., Burne, R.A. 2006. Influence of BrpA on critical virulence attributes of Streptococcus mutans. J Bacteriol. 188(8):2983-92.
Windsor, A.J., Mitchell-Olds, T. 2006. Comparative genomics as a tool for gene discovery. Current Opinion in Biotechnology. 17:161-7.
Wittkopp, P.J., Kalay, G. 2012. Cis-regulatory elements: Molecular mechanisms and evolutionary processes underlying divergence. Nature Reviews Genetics. 13:59-69.
Yan, L., Helguera, M., Kato, K., Fukuyama, S., Sherman, J., Dubcovsky, J. 2004. Allelic variation at the VRN-1 promoter region in polyploid wheat. Theoretical and Applied Genetics. 109(8):1677-86.
Zeidan, A.A., Poulsen, V.K., Janzen, T., Buldo, P., Derkx, P.M.F., Øregaard, G., Neves, A.R. 2017. Polysaccharide production by lactic acid bacteria: from genes to industrial applications. FEMS Microbiology Reviews. 47.
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