In Silico Detection of Genetic Determinants for the Acquired Antibiotic Resistance and Biologically Active Compounds of Lactic Acid Bacteria from the Human Oral Microbiome
Abstract
1. Introduction
2. Materials and Methods
2.1. Microorganism Strains
2.2. Phenotypic Antibiotic Resistance
2.3. DNA Isolation
2.4. Whole-Genome Sequencing
2.5. Bioinformatics Processing
3. Results
3.1. Antibiotic Resistance and Detection of Acquired Genes
3.2. Detection of Genetic Determinants for Peptidase Activity
3.3. Detection of Genetic Determinants for Adhesion Proteins
3.4. Detection of Genetic Determinants for Bacteriocin Production
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Carr, F.J.; Chill, D.; Maida, N. The lactic acid bacteria: A literature survey. Crit. Rev. Microbiol. 2002, 28, 281–370. [Google Scholar] [CrossRef]
- Saez-Lara, M.J.; Gomez-Llorente, C.; Plaza-Diaz, J.; Gil, A. The Role of Probiotic Lactic Acid Bacteria and Bifidobacteria in the Prevention and Treatment of Inflammatory Bowel Disease and Other Related Diseases: A Systematic Review of Randomized Human Clinical Trials. Biomed. Res. Int. 2015, 2015, 505878. [Google Scholar] [CrossRef] [PubMed]
- Ren, C.; Faas, M.M.; de Vos, P. Disease managing capacities and mechanisms of host effects of lactic acid bacteria. Crit. Rev. Food Sci. Nutr. 2021, 61, 1365–1393. [Google Scholar] [CrossRef] [PubMed]
- Lai, W.K.; Lu, Y.C.; Hsieh, C.R.; Wei, C.K.; Tsai, Y.H.; Chang, F.R.; Chan, Y. Developing Lactic Acid Bacteria as an Oral Healthy Food. Life 2021, 11, 268. [Google Scholar] [CrossRef]
- Gad, G.F.; Abdel-Hamid, A.M.; Farag, Z.S. Antibiotic resistance in lactic acid bacteria isolated from some pharmaceutical and dairy products. Braz. J. Microbiol. 2014, 45, 25–33. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Zhang, Q. Relationship between tetracycline antibiotic susceptibility and genotype in oral cavity Lactobacilli clinical isolates. Antimicrob. Resist. Infect. Control 2019, 8, 27. [Google Scholar] [CrossRef]
- Roberts, A.P.; Kreth, J. The impact of horizontal gene transfer on the adaptive ability of the human oral microbiome. Front. Cell. Infect. Microbiol. 2014, 4, 124. [Google Scholar] [CrossRef]
- Hayek, S.; Ibrahim, S. Current Limitations and Challenges with Lactic Acid Bacteria: A Review. Food Nutri. Sci. 2013, 4, 73–87. [Google Scholar] [CrossRef]
- Kieliszek, M.; Pobiega, K.; Piwowarek, K.; Kot, A.M. Characteristics of the Proteolytic Enzymes Produced by Lactic Acid Bacteria. Molecules 2021, 26, 1858. [Google Scholar] [CrossRef]
- Christensen, J.; Dudley, E.; Pederson, J.; Steele, J. Peptidases and amino acid catabolism in lactic acid bacteria. Anton. Leeuw. 1999, 76, 217–246. [Google Scholar] [CrossRef]
- Wang, Y.; Wu, J.; Lv, M.; Shao, Z.; Hungwe, M.; Wang, J.; Bai, X.; Xie, J.; Wang, Y.; Geng, W. Metabolism Characteristics of Lactic Acid Bacteria and the Expanding Applications in Food Industry. Front. Bioeng. Biotechnol. 2021, 9, 612285. [Google Scholar] [CrossRef] [PubMed]
- Koryszewska-Bagińska, A.; Gawor, J.; Nowak, A.; Grynberg, M.; Aleksandrzak-Piekarczyk, T. Comparative genomics and functional analysis of a highly adhesive dairy Lactobacillus paracasei subsp. paracasei IBB3423 strain. Appl. Microbiol. Biotechnol. 2019, 103, 7617–7634. [Google Scholar] [CrossRef] [PubMed]
- Styriak, I.; Nemcova, R.; Chang, Y.-H.; Ljungh, A. Binding of extracellular matrix molecules by probiotic bacteria. Lett. Appl. Microbiol. 2003, 37, 329–333. [Google Scholar] [CrossRef]
- Muscariello, L.; De Siena, B.; Marasco, R. Lactobacillus Cell Surface Proteins Involved in Interaction with Mucus and Extracellular Matrix Components. Curr. Microbiol. 2020, 77, 3831–3841. [Google Scholar] [CrossRef] [PubMed]
- Lebeer, S.; Vanderleyden, J.; De Keersmaecker, S.C. Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 2008, 72, 728–764. [Google Scholar] [CrossRef]
- Dawid, S.; Roche, A.M.; Weiser, J.N. The blp bacteriocins of Streptococcus pneumoniae mediate intraspecies competition both in vitro and in vivo. Infect. Immun. 2007, 75, 443–451. [Google Scholar] [CrossRef]
- Zacharof, M.P.; Lovitt, R.W. Bacteriocins produced by lactic acid bacteria a review article. APCBEE Procedia. 2012, 2, 50–56. [Google Scholar] [CrossRef]
- Hassan, M.U.; Nayab, H.; Rehman, T.U.; Williamson, M.P.; Haq, K.U.; Shafi, N.; Shafique, F. Characterisation of Bacteriocins Produced by Lactobacillus spp. Isolated from the Traditional Pakistani Yoghurt and Their Antimicrobial Activity against Common Foodborne Pathogens. Biomed. Res. Int. 2020, 2020, 8281623. [Google Scholar] [CrossRef]
- Darbandi, A.; Asadi, A.; Mahdizade Ari, M.; Ohadi, E.; Talebi, M.; Halaj Zadeh, M.; Darb Emamie, A.; Ghanavati, R.; Kakanj, M. Bacteriocins: Properties and potential use as antimicrobials. J. Clin. Lab. Anal. 2022, 36, e24093. [Google Scholar] [CrossRef]
- Solis-Balandra, M.A.; Sanchez-Salas, J.L. Classification and Multi-Functional Use of Bacteriocins in Health, Biotechnology, and Food Industry. Antibiotics 2024, 13, 666. [Google Scholar] [CrossRef]
- Alvarez-Sieiro, P.; Montalbán-López, M.; Mu, D.; Kuipers, O.P. Bacteriocins of lactic acid bacteria: Extending the family. Appl. Microbiol. Biotechnol. 2016, 100, 2939–2951. [Google Scholar] [CrossRef]
- Mendoza, R.M.; Kim, S.H.; Vasquez, R.; Hwang, I.C.; Park, Y.S.; Paik, H.D.; Moon, G.S.; Kang, D.K. Bioinformatics and its role in the study of the evolution and probiotic potential of lactic acid bacteria. Food Sci. Biotechnol. 2022, 32, 389–412. [Google Scholar] [CrossRef] [PubMed]
- Carriço, J.A.; Rossi, M.; Moran-Gilad, J.; Van Domselaar, G.; Ramirez, M. A primer on microbial bioinformatics for nonbioinformaticians. Clin. Microbiol. Infect. 2018, 24, 342–349. [Google Scholar] [CrossRef]
- Kahraman-Ilıkkan, Ö. Comparative genomics of four lactic acid bacteria identified with Vitek MS (MALDI-TOF) and whole-genome sequencing. Mol. Genet. Genomics. 2024, 299, 31. [Google Scholar] [CrossRef]
- Syrokou, M.K.; Paramithiotis, S.; Drosinos, E.H.; Bosnea, L.; Mataragas, M. A Comparative Genomic and Safety Assessment of Six Lactiplantibacillus plantarum subsp. argentoratensis Strains Isolated from Spontaneously Fermented Greek Wheat Sourdoughs for Potential Biotechnological Application. Int. J. Mol. Sci. 2022, 23, 2487. [Google Scholar] [CrossRef]
- Stergiou, O.S.; Tegopoulos, K.; Kiousi, D.E.; Tsifintaris, M.; Papageorgiou, A.C.; Tassou, C.C.; Chorianopoulos, N.; Kolovos, P.; Galanis, A. Whole-Genome Sequencing, Phylogenetic and Genomic Analysis of Lactiplantibacillus pentosus L33, a Potential Probiotic Strain Isolated from Fermented Sausages. Front. Microbiol. 2021, 12, 746659. [Google Scholar] [CrossRef] [PubMed]
- Atanasov, N.; Evstatieva, Y.; Nikolova, D. Probiotic Potential of Lactic Acid Bacterial Strains Isolated from Human Oral Microbiome. Microbiol. Res. 2023, 14, 262–278. [Google Scholar] [CrossRef]
- Goo, R.-Y.; Li, M.-S. Proposal of Sphingobacterium allocomposti nom. nov., Mycobacterium chelonae subsp. bovistauri nom. nov. and Lactobacillus delbrueckii subsp. allosunkii nom. nov. as new names with replacement specific or subspecific epithets, respectively, for three illegitimate prokaryotic names Sphingobacterium composti Yoo et al. 2007, Mycobacterium chelonae subsp. bovis Kim et al. 2017 and Lactobacillus delbrueckii subsp. sunkii Kudo et al. 2012; proposal of Christiangramia oceanisediminis comb. nov. and Christiangramia crocea comb. nov. as replacement names respectively for two illegitimate prokaryotic names Gramella oceanisediminis Yang et al. 2023 and Gramella crocea Zhang et al. 2023. Int. J. Syst. Evol. Microbiol. 2024, 74, 006319. [Google Scholar] [CrossRef]
- Bauer, A.W.; Kirby, W.M.; Sherris, J.C.; Turck, M. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 1966, 45, 493–496. [Google Scholar] [CrossRef]
- Jorgensen, J.; Turnidge, J. Susceptibility Test Methods: Dilution and Disk Diffusion Methods. In Manual of Clinical Microbiology, 10th ed.; Versalovic, J., Carroll, K.C., Funke, G., Jorgensen, J.H., Landry, M.L., Warnock, D.W., Eds.; ASM Press: Washington, DC, USA, 2015; pp. 1253–1273. [Google Scholar] [CrossRef]
- CLSI. Performance Standards for Antimicrobial Susceptibility Testing, 30th ed.; CLSI supplement M100; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2020. [Google Scholar]
- Gökmen, G.G.; Sarıyıldız, S.; Cholakov, R.; Nalbantsoy, A.; Baler, B.; Aslan, E.; Düzel, A.; Sargın, S.; Göksungur, Y.; Kışla, D. A novel Lactiplantibacillus plantarum strain: Probiotic properties and optimization of the growth conditions by response surface methodology. World J. Microbiol. Biotechnol. 2024, 40, 66. [Google Scholar] [CrossRef]
- Andrews, S. FastQC: A Quality Control Tool for High throughput Sequence Data. 2010. Available online: https://www.bioinformatics.babraham.ac.uk/projects/fastqc/ (accessed on 24 July 2024).
- Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [Google Scholar] [CrossRef] [PubMed]
- Seemann, T. Shovill. 2019. Available online: https://github.com/tseemann/shovill (accessed on 24 July 2024).
- Gurevich, A.; Saveliev, V.; Vyahhi, N.; Tesler, G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics 2013, 29, 1072–1075. [Google Scholar] [CrossRef]
- Seemann, T. ABRicate: Mass Screening of Contigs for Antimicrobial Resistance or Virulence Genes. 2020. Available online: https://github.com/tseemann/abricate (accessed on 24 July 2024).
- Gertz, E.M.; Yu, Y.K.; Agarwala, R.; Schäffer, A.A.; Altschul, S.F. Composition-based statistics and translated nucleotide searches: Improving the TBLASTN module of BLAST. BMC Biol. 2006, 4, 41. [Google Scholar] [CrossRef]
- van Heel, A.J.; de Jong, A.; Song, C.; Viel, J.H.; Kok, J.; Kuipers, O.P. BAGEL4: A user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic Acids Res. 2018, 46, W278–W281. [Google Scholar] [CrossRef]
- EFSA. Guidance on the characterization of microorganisms used as feed additives or as production organisms. EFSA J. 2018, 16, e05206. [Google Scholar] [CrossRef]
- Van Tassell, M.L.; Miller, M.J. Lactobacillus Adhesion to Mucus. Nutrients 2011, 3, 613–636. [Google Scholar] [CrossRef] [PubMed]
- Juge, N. Microbial adhesins to gastrointestinal mucus. Trends Microbiol. 2012, 20, 30–39. [Google Scholar] [CrossRef] [PubMed]
- Etzold, S.; Juge, N. Structural insights into bacterial recognition of intestinal mucins. Curr. Opin. Struct. Biol. 2014, 28, 23–31. [Google Scholar] [CrossRef]
- Anisimova, E.A.; Yarullina, D.R. Antibiotic Resistance of Lactobacillus Strains. Curr. Microbiol. 2019, 76, 1407–1416. [Google Scholar] [CrossRef]
- Zhang, S.; Oh, J.H.; Alexander, L.M.; Özçam, M.; van Pijkeren, J.P. d-Alanyl-d-Alanine Ligase as a Broad-Host-Range Counterselection Marker in Vancomycin-Resistant Lactic Acid Bacteria. J. Bacteriol. 2018, 200, e00607–e00617. [Google Scholar] [CrossRef]
- Dec, M.; Nowaczek, A.; Stępień-Pyśniak, D.; Wawrzykowski, J.; Urban-Chmiel, R. Identification and antibiotic susceptibility of lactobacilli isolated from turkeys. BMC Microbiol. 2018, 18, 168. [Google Scholar] [CrossRef] [PubMed]
- Duskova, M.; Moravkova, M.; Mrazek, J.; Florianova, M.; Vorlova, L.; Karpiskova, R. Assessment of antibiotic resistance in starter and non-starter lactobacilli of food origin. Acta Vet. Brno. 2020, 89, 401–411. [Google Scholar] [CrossRef]
- Ammor, M.S.; Flórez, A.B.; Mayo, B. Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacteria. Food Microbiol. 2007, 24, 559–570. [Google Scholar] [CrossRef] [PubMed]
- Duche, R.T.; Singh, A.; Wandhare, A.G.; Sangwan, V.; Sihag, M.K.; Nwagu, T.N.T.; Panwar, H.; Ezeogu, L.I. Antibiotic resistance in potential probiotic lactic acid bacteria of fermented foods and human origin from Nigeria. BMC Microbiol. 2023, 23, 142. [Google Scholar] [CrossRef] [PubMed]
- Li, S.; Li, Z.; Wei, W.; Ma, C.; Song, X.; He, W.; Tian, J.; Huo, X. Association of mutation patterns in gyrA and ParC genes with quinolone resistance levels in lactic acid bacteria. J. Antibiot. 2015, 68, 81–87. [Google Scholar] [CrossRef]
- Zarzecka, U.; Chajęcka-Wierzchowska, W.; Zadernowska, A. Microorganisms from starter and protective cultures—Occurrence of antibiotic resistance and conjugal transfer of tet genes in vitro and during food fermentation. LWT 2022, 153, 112490. [Google Scholar] [CrossRef]
- Danielsen, M.; Wind, A. Susceptibility of Lactobacillus spp. to antimicrobial agents. Int. J. Food Microbiol. 2003, 82, 1–11. [Google Scholar] [CrossRef]
- Sharma, C.; Gulati, S.; Thakur, N.; Singh, B.P.; Gupta, S.; Kaur, S.; Mishra, S.K.; Puniya, A.K.; Gill, J.P.S.; Panwar, H. Antibiotic sensitivity pattern of indigenous lactobacilli isolated from curd and human milk samples. 3 Biotech 2017, 7, 53. [Google Scholar] [CrossRef]
- Delgado, S.; Flórez, A.B.; Mayo, B. Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr. Microbiol. 2005, 50, 202–207. [Google Scholar] [CrossRef]
- Zhou, J.S.; Pillidge, C.J.; Gopal, P.K.; Gill, H.S. Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int. J. Food. Microbiol. 2005, 98, 211–217. [Google Scholar] [CrossRef]
- Selvin, J.; Maity, D.; Sajayan, A.; Kiran, G.S. Revealing antibiotic resistance in therapeutic and dietary probiotic supplements. J. Glob. Antimicrob. Resist. 2020, 22, 202–205. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Dong, J.; Wang, J.; Chi, W.; Zhou, W.; Tian, Q.; Hong, Y.; Zhou, X.; Ye, H.; Tian, X.; et al. Assessing the drug resistance profiles of oral probiotic lozenges. J. Oral. Microbiol. 2022, 14, 2019992. [Google Scholar] [CrossRef]
- Dimitrov, Z.; Chorbadjiyska, E.; Gotova, I.; Pashova, K.; Ilieva, S. Selected adjunct cultures remarkably increase the content of bioactive peptides in Bulgarian white brined cheese. Biotechnol. Biotechnol. Equip. 2015, 29, 78–83. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Xu, M.; Hu, S.; Zhao, H.; Zhang, B. The Enzyme Gene Expression of Protein Utilization and Metabolism by Lactobacillus helveticus CICC 22171. Microorganisms 2022, 10, 1724. [Google Scholar] [CrossRef]
- Falasconi, I.; Fontana, A.; Patrone, V.; Rebecchi, A.; Duserm Garrido, G.; Principato, L.; Callegari, M.L.; Spigno, G.; Morelli, L. Genome-Assisted Characterization of Lactobacillus fermentum, Weissella cibaria, and Weissella confusa Strains Isolated from Sorghum as Starters for Sourdough Fermentation. Microorganisms 2020, 8, 1388. [Google Scholar] [CrossRef]
- Grizon, A.; Theil, S.; Helinck, S.; Gerber, P.; Bonnarme, P.; Chassard, C. Genomic Characterization of Wild Lactobacillus delbrueckii Strains Reveals Low Diversity but Strong Typicity. Microorganisms 2024, 12, 512. [Google Scholar] [CrossRef] [PubMed]
- Kiousi, D.E.; Efstathiou, C.; Tegopoulos, K.; Mantzourani, I.; Alexopoulos, A.; Plessas, S.; Kolovos, P.; Koffa, M.; Galanis, A. Genomic Insight into Lacticaseibacillus paracasei SP5, Reveals Genes and Gene Clusters of Probiotic Interest and Biotechnological Potential. Front. Microbiol. 2022, 13, 922689. [Google Scholar] [CrossRef]
- Vélez, M.P.; De Keersmaecker, S.C.; Vanderleyden, J. Adherence factors of Lactobacillus in the human gastrointestinal tract. FEMS Microbiol. Lett. 2007, 276, 140–148. [Google Scholar] [CrossRef]
- Nishiyama, K.; Sugiyama, M.; Mukai, T. Adhesion Properties of Lactic Acid Bacteria on Intestinal Mucin. Microorganisms 2016, 4, 34. [Google Scholar] [CrossRef]
- Patel, S.; Mathivanan, N.; Goyal, A. Bacterial adhesins, the pathogenic weapons to trick host defense arsenal. Biomed. Pharmacother. 2017, 93, 763–771. [Google Scholar] [CrossRef]
- Brinster, S.; Furlan, S.; Serror, P. C-terminal WxL domain mediates cell wall binding in Enterococcus faecalis and other gram-positive bacteria. J. Bacteriol. 2007, 189, 1244–1253. [Google Scholar] [CrossRef]
- Tsuchiya, W.; Fujimoto, Z.; Inagaki, N.; Nakagawa, H.; Tanaka, M.; Kimoto-Nira, H.; Yamazaki, T.; Suzuki, C. Cell-surface protein YwfG of Lactococcus lactis binds to α-1,2-linked mannose. PLoS ONE 2023, 18, e0273955. [Google Scholar] [CrossRef] [PubMed]
- Atanasov, N.; Evstatieva, Y.; Nikolova, D. Antagonistic Interactions of Lactic Acid Bacteria from Human Oral Microbiome against Streptococcus mutans and Candida albicans. Microorganisms 2023, 11, 1604. [Google Scholar] [CrossRef]
- Turner, M.S.; Hafner, L.M.; Walsh, T.; Giffard, P.M. Peptide surface display and secretion using two LPXTG-containing surface proteins from Lactobacillus fermentum BR11. Appl. Environ. Microbiol. 2003, 69, 5855–5863. [Google Scholar] [CrossRef]
- Germond, J.E.; Delley, M.; Gilbert, C.; Atlan, D. Determination of the domain of the Lactobacillus delbrueckii subsp. bulgaricus cell surface proteinase PrtB involved in attachment to the cell wall after heterologous expression of the prtB gene in Lactococcus lactis. Appl. Environ. Microbiol. 2003, 69, 3377–3384. [Google Scholar] [CrossRef] [PubMed]
- Chatterjee, M.; Pushkaran, A.C.; Vasudevan, A.K.; Menon, K.K.N.; Biswas, R.; Mohan, C.G. Understanding the adhesion mechanism of a mucin binding domain from Lactobacillus fermentum and its role in enteropathogen exclusion. Int. J. Biol. Macromol. 2018, 110, 598–607. [Google Scholar] [CrossRef] [PubMed]
- de Jesus, L.C.L.; Drumond, M.M.; Aburjaile, F.F.; Sousa, T.J.; Coelho-Rocha, N.D.; Profeta, R.; Brenig, B.; Mancha-Agresti, P.; Azevedo, V. Probiogenomics of Lactobacillus delbrueckii subsp. lactis CIDCA 133: In Silico, In Vitro, and In Vivo Approaches. Microorganisms 2021, 9, 829. [Google Scholar] [CrossRef]
- Batista, V.L.; De Jesus, L.C.L.; Tavares, L.M.; Barroso, F.L.A.; Fernandes, L.J.D.S.; Freitas, A.D.S.; Americo, M.F.; Drumond, M.M.; Mancha-Agresti, P.; Ferreira, E.; et al. Paraprobiotics and Postbiotics of Lactobacillus delbrueckii CIDCA 133 Mitigate 5-FU-Induced Intestinal Inflammation. Microorganisms 2022, 10, 1418. [Google Scholar] [CrossRef]
- McAnulty, M.J.; Guron, G.K.; Oest, A.M.; Miller, A.L.; Renye, J.A., Jr. The quorum sensing peptide BlpC regulates the transcription of genes outside its associated gene cluster and impacts the growth of Streptococcus thermophilus. Front. Microbiol. 2024, 14, 1304136. [Google Scholar] [CrossRef]
- Cui, Y.; Zhang, C.; Wang, Y.; Shi, J.; Zhang, L.; Ding, Z.; Qu, X.; Cui, H. Class IIa bacteriocins: Diversity and new developments. Int. J. Mol. Sci. 2012, 13, 16668–16707. [Google Scholar] [CrossRef]
- Etayash, H.; Norman, L.; Thundat, T.; Stiles, M.; Kaur, K. Surface-conjugated antimicrobial peptide leucocin a displays high binding to pathogenic gram-positive bacteria. ACS Appl. Mater. Interfaces 2014, 6, 1131–1138. [Google Scholar] [CrossRef] [PubMed]
- Mathiesen, G.; Huehne, K.; Kroeckel, L.; Axelsson, L.; Eijsink, V.G. Characterization of a new bacteriocin operon in sakacin P-producing Lactobacillus sakei, showing strong translational coupling between the bacteriocin and immunity genes. Appl. Environ. Microbiol. 2005, 71, 3565–3574. [Google Scholar] [CrossRef] [PubMed]
- Delves-Broughton, J. Natural antimicrobials as additives and ingredients for the preservation of foods and beverages. In Natural Food Additives, Ingredients and Flavourings; Woodhead Publishing: Cambridge, UK, 2012; pp. 127–161. [Google Scholar] [CrossRef]
- Rivas, F.P.; Castro, M.P.; Vallejo, M.; Marguet, E.; Campos, C.A. Sakacin Q produced by Lactobacillus curvatus ACU-1: Functionality characterization and antilisterial activity on cooked meat surface. Meat Sci. 2014, 97, 475–479. [Google Scholar] [CrossRef]
- Belguesmia, Y.; Bendjeddou, K.; Kempf, I.; Boukherroub, R.; Drider, D. Heterologous Biosynthesis of Five New Class II Bacteriocins from Lactobacillus paracasei CNCM I-5369 With Antagonistic Activity Against Pathogenic Escherichia coli Strains. Front. Microbiol. 2020, 11, 1198. [Google Scholar] [CrossRef]
- Romyasamit, C.; Surachat, K.; Pattaranggoon, N.C.; Suksabay, P.; Permpoon, U.; Nam, T.-G.; Sornsenee, P. Phenotypic and Genomic Insights into Schleiferilactobacillus harbinensis WU01, a Candidate Probiotic with Broad-Spectrum Antimicrobial Activity Against ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter) Pathogens. Foods 2025, 14, 1161. [Google Scholar] [CrossRef]
- Lou, H.; Wang, J.; Wang, Y.; Gao, Y.; Wang, W. Protective effects of potential probiotics Lacticaseibacillus rhamnosus SN21-1 and Lactiplantibacillus plantarum SN21-2 against Salmonella typhimurium infection in broilers. Poult. Sci. 2024, 103, 104207. [Google Scholar] [CrossRef]
- Kandasamy, S.; Lee, K.H.; Yoo, J.; Yun, J.; Kang, H.B.; Kim, J.E.; Oh, M.H.; Ham, J.S. Whole genome sequencing of Lacticaseibacillus casei KACC92338 strain with strong antioxidant activity, reveals genes and gene clusters of probiotic and antimicrobial potential. Front. Microbiol. 2024, 15, 1458221. [Google Scholar] [CrossRef] [PubMed]
- Ibrahim, O.O. Classification of Antimicrobial Peptides Bacteriocins, and the Nature of Some Bacteriocins with Potential Applications in Food Safety and Bio-Pharmaceuticals. EC Microbiology 2019, 15.7, 591–608. [Google Scholar]
- Meng, F.; Zhu, X.; Zhao, H.; Nie, T.; Lu, F.; Lu, Z.; Lu, Y. A class III bacteriocin with broad-spectrum antibacterial activity from Lactobacillus acidophilus NX2-6 and its preservation in milk and cheese. Food Control 2021, 121, 107597. [Google Scholar] [CrossRef]
- Surachat, K.; Sangket, U.; Deachamag, P.; Chotigeat, W. In silico analysis of protein toxin and bacteriocins from Lactobacillus paracasei SD1 genome and available online databases. PLoS ONE 2017, 12, e0183548. [Google Scholar] [CrossRef]
- Mkadem, W.; Belguith, K.; Oussaief, O.; ElHatmi, H.; Indio, V.; Savini, F.; De Cesare, A.; Boudhrioua, N. Systematic approach to select lactic acid bacteria from spontaneously fermented milk able to fight Listeria monocytogens and Staphylococcus aureus. Food Biosci. 2022, 51, 102275. [Google Scholar] [CrossRef]
- Ghosh, S.; Sarangi, A.N.; Mukherjee, M.; Bhowmick, S.; Tripathy, S. Reanalysis of Lactobacillus paracasei Lbs2 Strain and Large-Scale Comparative Genomics Places Many Strains into Their Correct Taxonomic Position. Microorganisms 2019, 7, 487. [Google Scholar] [CrossRef] [PubMed]
- Moiseenko, K.V.; Begunova, A.V.; Savinova, O.S.; Glazunova, O.A.; Rozhkova, I.V.; Fedorova, T.V. Biochemical and Genomic Characterization of Two New Strains of Lacticaseibacillus paracasei Isolated from the Traditional Corn-Based Beverage of South Africa, Mahewu, and Their Comparison with Strains Isolated from Kefir Grains. Foods 2023, 12, 223. [Google Scholar] [CrossRef] [PubMed]
Strain | Antibiotics | MAR Index | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
AMP | CD | VA | CIP | TR | C | E | GEN | K | N | RD | S | TE | ||
N 2 | S | S | R | R | S | S | S | R | R | R | S | R | S | 0.462 |
N 4-5 | S | S | R | R | R | S | S | R | R | R | S | R | I | 0.538 |
AG 2-6 | S | S | R | R | R | S | S | R | R | R | R | R | S | 0.615 |
KG 12-1 | S | S | R | R | R | S | S | R | R | R | S | R | S | 0.538 |
TC 3-11 | S | S | R | R | S | S | S | I | R | R | S | R | S | 0.385 |
VG 1 | S | S | I | R | R | S | S | R | R | R | S | R | S | 0.462 |
VG 2 | S | S | I | R | R | S | S | R | R | R | S | R | S | 0.462 |
MK 13-1 | S | S | I | R | R | S | S | R | R | R | S | R | S | 0.462 |
NN 1 | S | S | R | R | R | S | S | R | R | R | R | R | S | 0.615 |
NA 1-8 | S | S | R | I | R | S | S | R | R | R | S | R | S | 0.462 |
NA 2-2 | S | S | R | R | I | S | S | R | R | R | S | R | S | 0.462 |
AV 2-1 | S | S | R | R | R | S | S | R | R | R | S | R | S | 0.538 |
Strain | pepA | pepC | pepF | pepQ | pepT | pepV |
---|---|---|---|---|---|---|
L. fermentum N 2 | + | + | + | |||
L. fermentum N 4-5 | + | + | + | |||
W. confusa AG 2-6 | + | + | + | + | ||
L. curvatus KG 12-1 | + | + | + | |||
L. fermentum TC 3-11 | + | + | ||||
L. delbrueckii subsp. allosunkii VG 1 | + | + | + | + | + | |
L. delbrueckii subsp. lactis VG 2 | + | + | ||||
L. delbrueckii subsp. lactis MK 13-1 | + | + | + | + | + | |
W. confusa NN 1 | + | + | + | + | ||
L. rhamnosus NA 1-8 | + | |||||
L. fermentum NA 2-2 | + | + | + | |||
L. paracasei AV 2-1 | + | + | + |
Adhesin | Strain |
---|---|
KxYKxGKxW signal peptide domain-containing protein | L. fermentum N 2; L. fermentum N 4-5; W. confusa AG 2-6; L. fermentum TC 3-11; W. confusa NN 1; L. rhamnosus NA 1-8; L. fermentum NA 2-2 |
LPxTG cell wall anchor domain-containing protein | All studied strains |
MucBP domain-containing protein | L. fermentum N 2; W. confusa AG 2-6; L. curvatus KG 12-1; L. fermentum TC 3-11; W. confusa NN 1; L. rhamnosus NA 1-8; L. fermentum NA 2-2; L. paracasei AV 2-1 |
SEC 10/PgrA surface exclusion domain-containing protein | L. fermentum N 2; L. fermentum N 4-5; L. fermentum TC 3-11; L. delbrueckii subsp. allosunkii VG 1; L. delbrueckii subsp. lactis VG 2; L. delbrueckii subsp. lactis MK 13-1; L. fermentum NA 2-2; L. paracasei AV 2-1 |
YSIRK-type signal peptide-containing protein | L. fermentum N 2; L. fermentum N 4-5; L. fermentum TC 3-11; L. delbrueckii subsp. allosunkii VG 1; L. delbrueckii subsp. lactis VG 2; L. delbrueckii subsp. lactis MK 13-1; L. fermentum NA 2-2 |
Lectin | Strain |
---|---|
WxL domain-containing protein | W. confusa AG 2-6; L. curvatus KG 12-1; W. confusa NN 1; L. rhamnosus NA 1-8; L. paracasei AV 2-1 |
L-type lectin-domain-containing protein | W. confusa AG 2-6; W. confusa NN 1; L. paracasei AV 2-1 |
Strain | Detected Bacteriocin-Encoding Genetic Determinants | |
---|---|---|
NCBI BLASTx | BAGEL4 | |
L. fermentum N 2 | ND | ND |
L. fermentum N 4-5 | ND | ND |
W. confusa AG 2-6 | ND | ND |
L. curvatus KG 12-1 | Blp family class II bacteriocin; | Sakacin Q; |
leucocin A/sakacin P family class II bacteriocin | Sakacin P | |
L. fermentum TC 3-11 | ND | ND |
L. delbrueckii subsp. allosunkii VG 1 | helveticin J family class III bacteriocin | Helveticin J |
L. delbrueckii subsp. lactis VG 2 | helveticin J family class III bacteriocin | Helveticin J |
L. delbrueckii subsp. lactis MK 13-1 | helveticin J family class III bacteriocin | ND |
W. confusa NN 1 | ND | ND |
L. rhamnosus NA 1-8 | class IIb bacteriocin, lactobin A/cerein 7B family | Carnocin CP52; |
LSEI 2386; | ||
Enterocin Xβ | ||
L. fermentum NA 2-2 | ND | ND |
L. paracasei AV 2-1 | Blp family class II bacteriocin | Carnocin CP52; |
Enterolysin A; | ||
LSEI 2386; | ||
Enterocin Xβ |
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Atanasov, N.; Evstatieva, Y.; Nikolova, D. In Silico Detection of Genetic Determinants for the Acquired Antibiotic Resistance and Biologically Active Compounds of Lactic Acid Bacteria from the Human Oral Microbiome. Appl. Microbiol. 2025, 5, 60. https://doi.org/10.3390/applmicrobiol5030060
Atanasov N, Evstatieva Y, Nikolova D. In Silico Detection of Genetic Determinants for the Acquired Antibiotic Resistance and Biologically Active Compounds of Lactic Acid Bacteria from the Human Oral Microbiome. Applied Microbiology. 2025; 5(3):60. https://doi.org/10.3390/applmicrobiol5030060
Chicago/Turabian StyleAtanasov, Nikola, Yana Evstatieva, and Dilyana Nikolova. 2025. "In Silico Detection of Genetic Determinants for the Acquired Antibiotic Resistance and Biologically Active Compounds of Lactic Acid Bacteria from the Human Oral Microbiome" Applied Microbiology 5, no. 3: 60. https://doi.org/10.3390/applmicrobiol5030060
APA StyleAtanasov, N., Evstatieva, Y., & Nikolova, D. (2025). In Silico Detection of Genetic Determinants for the Acquired Antibiotic Resistance and Biologically Active Compounds of Lactic Acid Bacteria from the Human Oral Microbiome. Applied Microbiology, 5(3), 60. https://doi.org/10.3390/applmicrobiol5030060