Comparative genomics study of Lactobacillus plantarum strains provides perspectives about proteins involved in the probiogenomics / Estudo de genômica comparativa de cepas de Lactobacillus plantarum fornece perspectivas sobre proteínas envolvidas com probiogenômica

Carlos Leonardo Araújo, Samuel Amaral, Tayná Novaes, Géssica Faial, Larissa Dias, Ingrid Coutinho


Probiotic bacteria have received great attention in recent years due to the benefits conferred by this group of microorganisms on human health, such as the improvement of nutrient bioavailability, inhibiting the opportunistic pathogens growth and increasing host immune activity. In this context, the combination of Lactobacillus plantarum potential and the advent of NGS platforms contributed to the increase of genomes belonging to the species in the past decade. The present study aimed to use a series of bioinformatics tools to perform the comparative analysis of 41 completed genomes of the species. Genes involved in probiogenomics of the species were identified in the core genome, such as adhesion, antagonism to pathogens and host microbiota alterations. It was also detected a structural variation at genomic level, due to the identification of gene clusters present in certain strains and absent in others, a fact that may be related to the heterogeneity of habitats that L. plantarum can be isolated. Therefore, this study was able to provide new insights regarding the gene content of this important group of lactic acid bacteria, through the direct comparison of several strains, which opens the way for future studies aiming to understand the mechanisms by which L. plantarum is capable of causing its beneficial effects on human health.



Lactobacillus plantarum, pan-genomics, phylogenomics, probiotics

Full Text:



Guo W, Jia W, Li Y, Chen S (2010). Performances of Lactobacillus brevis for Producing Lactic Acid from Hydrolysate of Lignocellulosics. Appl Biochem Biotechnol 161:124 – 136.

E. Mani-López, E. Palou, A. López-Malo (2014). Probiotic viability and storage stability of yogurts and fermented milks prepared with several mixtures of lactic acid bacteria. J Dairy Sci 97(5):2578 – 257890.

Reddy LV, Park J, Wee Y (2015). Homofermentative Production of Optically Pure L-lactic Acid from Sucrose and Mixed Sugars by Batch Fermentation of Enterococcus faecalis RKY1. Biotechnol. Bioprocess Eng 20(6):1099 – 1105.

Perez RH, Zendo T, Sonomoto K (2014). Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microb Cell Fact. 13(Suppl 1):S3.

Campana R, Hemert S Van, Baffone W (2017). Strain?specific probiotic properties of lactic acid bacteria and their interference with human intestinal pathogens invasion. Gut Pathog 6:1 – 12. 10.1186/s13099-017-0162-4

Mahato NK, Gupta V, Singh P, Kumari R, Verma H, Tripathi C, et al (2017). Microbial taxonomy in the era of OMICS: application of DNA sequences, computational tools and techniques. Antonie Van Leeuwenhoek 110(10):1357 – 1371.

Valerio F, Bellis P De, Lonigro SL, Visconti A, Lavermicocca P (2008). Use of Lactobacillus plantarum fermentation products in bread-making to prevent Bacillus subtilis ropy spoilage. Int J Food Microbiol 2008;122:328 – 332.

Jia F, Zhang L, Pang X, Gu X, Abdelazez A, Liang Y (2017). Complete genome sequence of bacteriocin-producing Lactobacillus plantarum KLDS1.0391, a probiotic strain with gastrointestinal tract resistance and adhesion to the intestinal epithelial cells. Genomics 109(5–6):432 – 437.

Landete JM, Rodríguez H, Curiel JA, Rivas B De, De FL (2010). Degradation of Phenolic Compounds Found in Olive Products by Lactobacillus plantarum Strains. In: Olives and Olive Oil in Health and Disease Prevention. Elsevier Inc.; 2010. p. 387 – 396.

Li P, Zhou Q, Gu Q (2016). Complete genome sequence of Lactobacillus plantarum LZ227, a potential probiotic strain producing B-group vitamins. J Biotechnol 234:66 – 70.

Altermann E, Russell WM, Azcarate-Peril MA, Barrangou R, Buck BL, Mcauliffe O, et al (2005). Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc Natl Acad Sci USA 15;102(11):3906 – 3912.

Siezen RJ, Tzeneva VA, Castioni A, Wels M, Phan HTK, Rademaker JLW, et al (2010). Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ Microbiol 12(3):758 – 773.

Kleerebezem M, Boekhorst J, Kranenburg R Van, Molenaar D, Kuipers OP, Leer R, et al (2003). Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci USA 18;100(4):1990 – 1995.

Dhanani AS, Bagchi T (2013). Lactobacillus plantarum CS24.2 prevents Escherichia coli adhesion to HT?29 cells and also down?regulates enteropathogen?induced tumor necrosis factor-? and interleukin?8 expression. 2013. Microbiol Immunol 57(4):309 – /315. 10.1111/1348-0421.12038

Behera SS, Ray RC, Zdolec N (2018). Lactobacillus plantarum with Functional Properties: An Approach to Increase Safety and Shelf-Life of Fermented Foods. Biomed Res Int 2018: 1 – 19.

Neal-McKinney JM, Lu X, Duong T, Larson CL, Call DR, Shah DH, et al (2012). Production of Organic Acids by Probiotic Lactobacilli Can Be Used to Reduce Pathogen Load in Poultry. PLoS One 7(9):1 – 11.

Cortés-Zavaleta O, López-Malo A, Hernández-Mendoza A, García HS (2014). Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. Int J Food Microbiol 173:30 – 35.

Sabo S da S, Vitolo M, González JMD, Oliveira RP de S (2014). Overview of Lactobacillus plantarum as a promising bacteriocins producer among lactic acid bacteria. Food Res Int 64:527 – 536.

Park S, Seong K, Lim S (2016). Anti-obesity Effect of Yogurt Fermented by Lactobacillus plantarum Q180 in Diet-induced Obese Rats. Korean J Food Sci Anim Resour 36(1): 77 – 83.

Kim S, Huang E, Park S, Holzapfel W (2018). Physiological Characteristics and Anti-obesity Effect of Lactobacillus plantarum K10. Korean J Food Sci Anim Resour 38(3):554 – 569.

Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI (2008). Diet-Induced Obesity Is Linked to Marked but Reversible Alterations in the Mouse Distal Gut Microbiome. Cell Press 3(4):213 – 223.

Wu C-C, Weng W-L, Lai W-L, Tsai H-P, Liu W-H, Lee M-H, et al (2015). Effect of Lactobacillus plantarum Strain K21 on High-Fat-Diet-Fed Obese Mice. Evidence-Based Complement Altern Med. 2015:1 – 9.

Van Dijk EL, Jaszczyszyn Y, Naquin D, Thermes C (2018). The Third Revolution in Sequencing Technology. Trends Genet 34(9):666 - 681.

Vincent AT, Derome N, Boyle B, Culley AI, Charette SJ (2017). Next-generation sequencing (NGS) in the microbiological world: How to make the most of your money. J Microbiol Methods 138:60 – 71.

Golicz AA, Batley J, Edwards D (2016). Towards plant pangenomics. Plant Biotechnol J 14(4):1099 – 1105.

Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al (2014). The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 42(D1):206 – 214. 10.1093/nar/gkt1226

Pantoja Y, Pinheiro K, Veras A, Araújo F, Lopes de Sousa A, Guimarães LC, et al (2017). PanWeb: A web interface for pan-genomic analysis. PLoS One 12(5):e0178154.

Zhao Y, Wu J, Yang J, Sun S, Xiao J, Yu J (2012). PGAP: Pan-genomes analysis pipeline. Bioinformatics 28(3):416 – 418.

Snipen L, Liland KH (2015). micropan: an R-package for microbial pan-genomics. BMC Bioinformatics. 16(79):1 – 8.

Thompson JD, Higgins DG, Gibson TJ (1994). ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673 – 4680

Kumar S, Stecher G, Tamura K (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33(7):1870 – 1874.

Ågren J, Sundström A, Hafström T, Segerman B (2012). Gegenees: Fragmented Alignment of Multiple Genomes for Determining Phylogenomic Distances and Genetic Signatures Unique for Specified Target Groups. PLoS One 7(6):e39107.

Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA (2011). BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12(1):402 1 – 10.

Araujo FA, Barh D, Silva A, Guimarães L, Ramos RTJ (2018). GO FEAT: a rapid web-based functional annotation tool for genomic and transcriptomic data. Sci Rep 8(1):1794.

Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R (2005). The microbial pan-genome. Curr Opin Genet Dev 15(6):589 – 594.

Guimarães LC, de Jesus LB, Viana MVC, Silva A, Ramos RTJ, Soares S de C, et al (2015). Inside the Pan-genome - Methods and Software Overview. Curr Genomics 2015;16(4):245 – 252.

Guidone A, Zotta T, Ross RP, Stanton C, Rea MC, Parente E, et al (2014). Functional properties of Lactobacillus plantarum strains: A multivariate screening study. Food Sci Technol 2014;56(1):69 – 76.

Plengvidhya V, Breidt F, Lu Z, Fleming HP (2007). DNA Fingerprinting of Lactic Acid Bacteria in Sauerkraut Fermentations Appl Environ Microbiol 73(23):7697 – 702.

Luxananil P, Promchai R, Wanasen S, Kamdee S, Thepkasikul P, Plengvidhya V, et al (2009). Monitoring Lactobacillus plantarum BCC 9546 starter culture during fermentation of Nham, a traditional Thai pork sausage. Int J Food Microbiol 2009;129(3):312 – 315.

Siezen RJ, Et J, Vlieg VH (2011). Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb Cell Fact 2011;10(Suppl 1):S3.

Canchaya C, Fournous G, Brüssow H (2004). The impact of prophages on bacterial chromosomes. Mol Microbiol 53(1):9 – 18.

Lee CY, Iandolo JJ (1986). Lysogenic conversion of staphylococcal lipase is caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J Bacteriol 166(2):385 – 391.

Dubin MJ, Scheid OM, Becker C (2018). Transposons: a blessing curse. Curr Opin Plant Biol 42:23 – 29.

Aziz RK, Breitbart M, Edwards RA (2010). Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 2010;38(13):4207 – 4217.

Holo H, Jeknic Z, Daeschel M, Stevanovic S, Nes IF (2001). Plantaricin W from Lactobacillus plantarum belongs to a new family of two-peptide lantibiotics. Microbiology 147:643–51.

Cotter PD, Ross RP, Hill C (2012). Bacteriocins - a viable alternative to antibiotics? Nat Rev Microbiol 11(2):95–105.

Todorov SD (2009). Bacteriocins from Lactobacillus plantarum – Production, Genetic Organization and mode of action. Brazilian J Microbiol. 40:209 – 221.

Nwodo UU, Green E, Okoh AI (2012). Bacterial Exopolysaccharides: Functionality and Prospects. 13(11):14002 – 14015.

Castro-Bravo N, Wells JM, Margolles A, Ruas-Madiedo P (2018). Interactions of Surface Exopolysaccharides From Bifidobacterium and Lactobacillus Within the Intestinal Environment. Front Microbiol 9:1 – 15.

Vernikos G, Medini D, Riley DR, Tettelin H (2015). Ten years of pan-genome analyses. Curr Opin Microbiol 23:148 – 154.

Tettelin H, Riley D, Cattuto C, Medini D (2008). Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11(5):472 – 477.

Zhang W, Ji H, Zhang D, Liu H, Wang S, Wang J, et al (2018). Complete Genome Sequencing of Lactobacillus plantarum ZLP001, a Potential Probiotic That Enhances Intestinal Epithelial Barrier Function and Defense Against Pathogens in Pigs. Front Physiol 9:1 – 7.

De las Rivas B, Marcobal Á, Muñoz R (2006). Development of a multilocus sequence typing method for analysis of Lactobacillus plantarum strains. Microbiology 152:85 – 93.

Mercanti DJ, Rousseau GM, Capra ML, Quiberoni A, Tremblay DM, Labrie SJ (2016). Genomic Diversity of Phages Infecting Probiotic Strains of Lactobacillus paracasei. Appl Environ Microbiol 82(1):95 – 105.

Soucy SM, Huang J, Gogarten JP (2015). Horizontal gene transfer: building the web of life. Nat Rev Genet 16(8):472 – 482.

Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al (2000). Gene Ontology: Tool for the unification of biology. Nat Genet 25(1):25 – 29.

Watanabe M, Van der Veen S, Abee T (2012). Impact of Respiration on Resistance of Lactobacillus plantarum WCFS1 to Acid Stress. Appl Environ Microbiol 78(11):4062 – 4064.

Ventura M, Turroni F, Van Sinderen D (2012). Probiogenomics as a tool to obtain genetic insights into adaptation of probiotic bacteria to the human gut. Bioeng Bugs 3(2):73 – 79.

Ventura M, Flaherty SO, Claesson MJ, Turroni F, Klaenhammer D, Van Sinderen D, O’Toole PW (2009). Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7(1): 61 – 71.

Hegarty JW, Guinane CM, Ross RP, Hill C, Cotter PD (2016). Bacteriocin production: a relatively unharnessed probiotic trait ?. F1000Res 5: 2587.

Castaldo C, Vastano V, Siciliano RA, Candela M, Vici M, Muscariello L et al (2009). Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin binding protein. Microb Cell Fact 8:14.

Begley M, Hill C, Gahan CGM (2006). Bile Salt Hydrolase Activity in Probiotics. Appl Environ Microbiol 72(3):1729 – 1738.

Halder D, Mandal M, Chatterjee S, Pal N, Mandal S (2017). Indigenous Probiotic Lactobacillus Isolates Presenting Antibiotic like Activity against Human Pathogenic Bacteria. Biomedicines 5(2):31.

O’Flaherty S, Crawley AB, Theriot CM, Barrangou R (2018). The Lactobacillus Bile Salt Hydrolase Repertoire Reveals Niche-Specific Adaptation. mSphere. 3(3):1 – 13.