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Abstract

Species belonging to the family are found in highly diverse environments and play an important role in fermented foods and probiotic products. Many of these species have been individually reported to harbour plasmids that encode important genes. In this study, we performed comparative genomic analysis of publicly available data for 512 plasmids from 282 strains represented by 51 species of this family and correlated the genomic features of plasmids with the ecological niches in which these species are found. Two-thirds of the species had at least one plasmid-harbouring strain. Plasmid abundance and GC content were significantly lower in vertebrate-adapted species as compared to nomadic and free-living species. Hierarchical clustering highlighted the distinct nature of plasmids from the nomadic and free-living species than those from the vertebrate-adapted species. EggNOG-assisted functional annotation revealed that genes associated with transposition, conjugation, DNA repair and recombination, exopolysaccharide production, metal ion transport, toxin–antitoxin system, and stress tolerance were significantly enriched on the plasmids of the nomadic and in some cases nomadic and free-living species. On the other hand, genes related to anaerobic metabolism, ABC transporters and the major facilitator superfamily were overrepresented on the plasmids of the vertebrate-adapted species. These genomic signatures correlate with the comparatively nutrient-depleted, stressful and dynamic environments of nomadic and free-living species and nutrient-rich and anaerobic environments of vertebrate-adapted species. Thus, these results indicate the contribution of the plasmids in the adaptation of lactobacilli to their respective habitats. This study also underlines the potential application of these plasmids in improving the technological and probiotic properties of lactic acid bacteria.

Funding
This study was supported by the:
  • Erasmus+ (Award 598515-EPP-1-2018-1-IN-EPPKA2-CBHE-JP)
    • Principle Award Recipient: Not Applicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2020-11-09
2024-03-29
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References

  1. Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB et al. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae . Int J Syst Evol Microbiol 2020; 70:2782–2858 [View Article][PubMed]
    [Google Scholar]
  2. Slover CM. Lactobacillus: a Review. Clin Microbiol Newsl 2008; 30:23–27
    [Google Scholar]
  3. Evivie SE, Huo G-C, Igene JO, Bian X. Some current applications, limitations and future perspectives of lactic acid bacteria as probiotics. Food Nutr Res 2017; 61:1318034 [View Article][PubMed]
    [Google Scholar]
  4. Hatti-Kaul R, Chen L, Dishisha T, Enshasy HE, El EH. Lactic acid bacteria: from starter cultures to producers of chemicals. FEMS Microbiol Lett 2018; 365: [View Article][PubMed]
    [Google Scholar]
  5. Duar RM, Lin XB, Zheng J, Martino ME, Grenier T et al. Lifestyles in transition: evolution and natural history of the genus Lactobacillus . FEMS Microbiol Rev 2017; 41:S27–48 [View Article][PubMed]
    [Google Scholar]
  6. Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B et al. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci U S A 2006; 103:15611–15616 [View Article][PubMed]
    [Google Scholar]
  7. Zheng J, Guan Z, Cao S, Peng D, Ruan L et al. Plasmids are vectors for redundant chromosomal genes in the Bacillus cereus group. BMC Genomics 2015; 16:6 [View Article][PubMed]
    [Google Scholar]
  8. Danner H, Holzer M, Mayrhuber E, Braun R. Acetic acid increases stability of silage under aerobic conditions. Appl Environ Microbiol 2003; 69:562–567 [View Article][PubMed]
    [Google Scholar]
  9. O'Sullivan O, O'Callaghan J, Sangrador-Vegas A, McAuliffe O, Slattery L et al. Comparative genomics of lactic acid bacteria reveals a niche-specific gene set. BMC Microbiol 2009; 9:50 [View Article][PubMed]
    [Google Scholar]
  10. Martino ME, Bayjanov JR, Caffrey BE, Wels M, Joncour P et al. Nomadic lifestyle of Lactobacillus plantarum revealed by comparative genomics of 54 strains isolated from different habitats. Environ Microbiol 2016; 18:4974–4989 [View Article][PubMed]
    [Google Scholar]
  11. Gänzle MG. Lactic metabolism revisited: metabolism of lactic acid bacteria in food fermentations and food spoilage. Current Opinion in Food Science 2 Elsevier Ltd; 2015 pp 106–117
    [Google Scholar]
  12. Zheng J, Ruan L, Sun M, Gänzle M. A genomic view of lactobacilli and pediococci demonstrates that phylogeny matches ecology and physiology. Appl Environ Microbiol 2015; 81:7233–7243 [View Article][PubMed]
    [Google Scholar]
  13. Folli C, Levante A, Percudani R, Amidani D, Bottazzi S et al. Toward the identification of a type I toxin-antitoxin system in the plasmid DNA of dairy Lactobacillus rhamnosus . Sci Rep 2017; 7:1–13
    [Google Scholar]
  14. Zhai Z, Yang Y, Wang J, Wang G, Ren F et al. Complete genome sequencing of Lactobacillus plantarum CAUH2 reveals a novel plasmid pCAUH203 associated with oxidative stress tolerance. 3 Biotech 2019; 9:116 [View Article][PubMed]
    [Google Scholar]
  15. Cui Y, Hu T, Qu X, Zhang L, Ding Z et al. Plasmids from food lactic acid bacteria: diversity, similarity, and new developments. Int J Mol Sci 2015; 16:13172–13202 [View Article][PubMed]
    [Google Scholar]
  16. Song Y, He Q, Zhang J, Qiao J, Xu H et al. Genomic variations in probiotic Lactobacillus plantarum P-8 in the human and rat gut. Front Microbiol 2018; 9:893 [View Article][PubMed]
    [Google Scholar]
  17. D C, RP R GF. C S. Sequence analysis of the plasmid genome of the probiotic strain Lactobacillus paracasei NFBC338 Which Includes the Plasmids pCD01 and pCD02. Plasmid 2005; 54:
    [Google Scholar]
  18. Fraunhofer ME, Geißler AJ, Behr J, Vogel RF. Comparative genomics of Lactobacillus brevis reveals a significant plasmidome overlap of brewery and insect isolates. Curr Microbiol 2019; 76:37–47 [View Article][PubMed]
    [Google Scholar]
  19. Fallico V, McAuliffe O, Fitzgerald GF, Ross RP. Plasmids of raw milk cheese isolate Lactococcus lactis subsp. lactis biovar diacetylactis DPC3901 suggest a plant-based origin for the strain. Appl Environ Microbiol 2011; 77:6451–6462 [View Article][PubMed]
    [Google Scholar]
  20. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article][PubMed]
    [Google Scholar]
  21. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002; 30:1575–1584 [View Article][PubMed]
    [Google Scholar]
  22. Howe E, Holton K, Nair S, Schlauch D, Sinha R. Mev: Multiexperiment Viewer. In: Biomedical Informatics for Cancer Research Boston, MA: Springer US; 2010 pp 267–277
    [Google Scholar]
  23. Letunic I, Bork P. Interactive tree of life (iTOL) V3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–245 [View Article][PubMed]
    [Google Scholar]
  24. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics 2011; 27:1009–1010 [View Article][PubMed]
    [Google Scholar]
  25. Deo D, Davray D, Kulkarni R. A diverse repertoire of exopolysaccharide biosynthesis gene clusters in Lactobacillus revealed by comparative analysis in 106 sequenced genomes. Microorganisms 2019; 7:E444 [View Article][PubMed]
    [Google Scholar]
  26. Dietel A-K, Merker H, Kaltenpoth M, Kost C. Selective advantages favour high genomic AT-contents in intracellular elements. In Blokesch M. editor PLOS Genet 15(4) 2019 p e1007778
    [Google Scholar]
  27. Nishida H. Comparative analyses of base compositions, DNA sizes, and dinucleotide frequency profiles in archaeal and bacterial chromosomes and plasmids. Int J Evol Biol 2012; 2012:1–5 [View Article][PubMed]
    [Google Scholar]
  28. Lawrence JG, Ochman H. Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci U S A 1998; 95:9413–9417 [View Article][PubMed]
    [Google Scholar]
  29. Rocha EPC, Danchin A. Base composition bias might result from competition for metabolic resources. vol. 18, trends in genetics. Trends Genet 2002291–294
    [Google Scholar]
  30. Almpanis A, Swain M, Gatherer D, McEwan N. Correlation between bacterial G+C content, genome size and the G+C content of associated plasmids and bacteriophages. Microb genomics 2018; 4:
    [Google Scholar]
  31. Kelleher P, Mahony J, Bottacini F, Lugli GA, Ventura M et al. The Lactococcus lactis pan-Plasmidome. Front Microbiol 2019; 10:707 [View Article][PubMed]
    [Google Scholar]
  32. Górecki RK, Koryszewska-Bagińska A, Gołębiewski M, Żylińska J, Grynberg M et al. Adaptative potential of the Lactococcus lactis IL594 strain encoded in its 7 plasmids. PLoS One 2011; 6:e22238 [View Article][PubMed]
    [Google Scholar]
  33. Li J, Hua ZS, Huang LN, Li J, Shi SH et al. Microbial communities evolve faster in extreme environments. Sci Rep 2014; 4:6205 [View Article][PubMed]
    [Google Scholar]
  34. Nelson WC, Wollerman L, Bhaya D, Heidelberg JF. Analysis of insertion sequences in thermophilic cyanobacteria: exploring the mechanisms of establishing, maintaining, and withstanding high insertion sequence abundance. Appl Environ Microbiol 2011; 77:5458–5466 [View Article][PubMed]
    [Google Scholar]
  35. Cobo-Simón M, Tamames J. Relating genomic characteristics to environmental preferences and ubiquity in different microbial taxa. BMC Genomics 2017; 18:499 [View Article][PubMed]
    [Google Scholar]
  36. Acosta S, Carela M, Garcia-Gonzalez A, Gines M, Vicens L et al. DNA repair is associated with information content in bacteria, archaea, and DNA viruses. J Hered 2015; 106:644–659 [View Article][PubMed]
    [Google Scholar]
  37. Zhang X, Rogers M, Bierschenk D, Bonten MJM, Willems RJL et al. A LacI-Family Regulator Activates Maltodextrin Metabolism of Enterococcus faecium . In Manganelli R. editor PLoS One 8 2013e72285 [View Article]
    [Google Scholar]
  38. Bidart GN, Rodríguez-Díaz J, Pérez-Martínez G, Yebra MJ. The lactose operon from Lactobacillus casei is involved in the transport and metabolism of the human milk oligosaccharide core-2 N-acetyllactosamine. Sci Rep 2018; 8:1–12
    [Google Scholar]
  39. Beekwilder J, Marcozzi D, Vecchi S, de Vos R, Janssen P et al. Characterization of Rhamnosidases from Lactobacillus plantarum and Lactobacillus acidophilus . Appl Environ Microbiol 2009; 75:3447–3454 [View Article][PubMed]
    [Google Scholar]
  40. Lorca G, Reddy L, Nguyen A, Sun EI, Tseng J et al. Lactic acid bacteria: comparative genomic analyses of transport systems. Biotechnology of Lactic Acid Bacteria Novel Applications 2007 pp 73–87
    [Google Scholar]
  41. Elkins CA, Moser SA, Savage DC. Genes encoding bile salt hydrolases and conjugated bile salt transporters in Lactobacillus johnsonii 100-100 and other Lactobacillus species. Microbiology 2001; 147:3403–3412 [View Article][PubMed]
    [Google Scholar]
  42. Dhakephalkar PK, Chopade BA. High levels of multiple metal resistance and its correlation to antibiotic resistance in environmental isolates of Acinetobacter . Biometals 1994; 7:67–74 [View Article][PubMed]
    [Google Scholar]
  43. Jiang X-W, Cheng H, Zheng B-W, Li A, Lv L-X et al. Comparative genomic study of three species within the genus Ornithinibacillus, reflecting the adaption to different habitats. Gene 2016; 578:25–31 [View Article][PubMed]
    [Google Scholar]
  44. van Kranenburg R, Golic N, Bongers R, Leer RJ, de Vos WM et al. Functional analysis of three plasmids from Lactobacillus plantarum . Appl Environ Microbiol 2005; 71:1223–1230 [View Article][PubMed]
    [Google Scholar]
  45. Loukin SH, MMC K, Zhou XL, Haynes WJ, Kung C. Microbial K+ Channels. vol. 125, Journal of General Physiology The Rockefeller University Press; 2005 pp 521–527
    [Google Scholar]
  46. Merchant AT, Spatafora GA. A role for the DtxR family of metalloregulators in gram-positive pathogenesis. Mol Oral Microbiol 2014; 29:1–7 [View Article][PubMed]
    [Google Scholar]
  47. Yao W, Yang L, Shao Z, Xie L, Chen L. Identification of salt tolerance-related genes of Lactobacillus plantarum D31 and T9 strains by genomic analysis. Ann Microbiol 2020; 70:1–14
    [Google Scholar]
  48. Böhmer N, König S, Fischer L. A novel manganese starvation-inducible expression system for Lactobacillus plantarum . FEMS Microbiol Lett 2013; 342:37–44 [View Article][PubMed]
    [Google Scholar]
  49. Goulter-Thorsen RM, Taran E, Gentle IR, Gobius KS, Dykes GA. CsgA production by Escherichia coli O157:H7 alters attachment to abiotic surfaces in some growth environments. Appl Environ Microbiol 2011; 77:7339–7344 [View Article][PubMed]
    [Google Scholar]
  50. Kwak W, Kim K, Lee C, Lee C, Kang J et al. Comparative analysis of the complete genome of Lactobacillus plantarum GB-LP2 and potential candidate genes for host immune system enhancement. J Microbiol Biotechnol 2016; 26:684–692 [View Article][PubMed]
    [Google Scholar]
  51. Remus DM, van Kranenburg R, van Swam II, Taverne N, Bongers RS et al. Impact of 4 Lactobacillus plantarum capsular polysaccharide clusters on surface glycan composition and host cell signaling. Microb Cell Fact 2012; 11:149 [View Article][PubMed]
    [Google Scholar]
  52. Khalil ES, Abd Manap MY, Mustafa S, Alhelli AM, Shokryazdan P. Probiotic properties of exopolysaccharide-producing Lactobacillus strains isolated from tempoyak. Molecules 2018; 23:E398 [View Article][PubMed]
    [Google Scholar]
  53. Rendueles O, Garcia-Garcerà M, Néron B, Touchon M, Rocha EPC. Abundance and co-occurrence of extracellular capsules increase environmental breadth: implications for the emergence of pathogens. PLoS Pathog 2017; 13:e1006525 [View Article][PubMed]
    [Google Scholar]
  54. Kralj S, van Geel-Schutten GH, Dondorff MMG, Kirsanovs S, van der Maarel MJEC et al. Glucan synthesis in the genus Lactobacillus: isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology 2004; 150:3681–3690 [View Article][PubMed]
    [Google Scholar]
  55. Cohan FM, Kopac SM. Microbial Genomics: E. coli Relatives Out of Doors and Out of Body 21 Current Biology, Cell Press; 2011 pp R587–589
    [Google Scholar]
  56. Sengupta R, Altermann E, Anderson RC, McNabb WC, Moughan PJ et al. The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediators Inflamm 2013; 2013:237921 [View Article][PubMed]
    [Google Scholar]
  57. Vélez MP, De Keersmaecker SCJ, Vanderleyden J. Adherence factors of Lactobacillus in the human gastrointestinal tract. Vol. 276, FEMS microbiology letters. FEMS Microbiol Lett 2007140–148
    [Google Scholar]
  58. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP et al. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 2003; 100:1990–1995 [View Article][PubMed]
    [Google Scholar]
  59. Pandey DP, Gerdes K. Toxin-Antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res 2005; 33:966–976 [View Article][PubMed]
    [Google Scholar]
  60. Wüthrich D, Irmler S, Berthoud H, Guggenbühl B, Eugster E et al. Conversion of methionine to cysteine in Lactobacillus paracasei depends on the highly mobile cysK-ctl-cysE gene cluster. Front Microbiol 2018; 9:2415 [View Article][PubMed]
    [Google Scholar]
  61. Zhao S, Zhang Q, Hao G, Liu X, Zhao J et al. The protective role of glycine betaine in Lactobacillus plantarum ST-III against salt stress. Food Control 2014; 44:208–213
    [Google Scholar]
  62. Maresca D, Zotta T, Mauriello G. Adaptation to aerobic environment of Lactobacillus johnsonii/gasseri strains. Front Microbiol 2018; 9:157 [View Article][PubMed]
    [Google Scholar]
  63. Riedl RA, Atkinson SN, Burnett CML, Grobe JL, Kirby JR. The gut microbiome, energy homeostasis, and implications for hypertension. Curr Hypertens Rep 2017; 19:27 [View Article][PubMed]
    [Google Scholar]
  64. Zotta T, Parente E, Ricciardi A. Aerobic metabolism in the genus Lactobacillus: impact on stress response and potential applications in the food industry. Vol. 122, Journal of Applied Microbiology. Blackwell Publishing Ltd 2017857–869
    [Google Scholar]
  65. Chambellon E, Rijnen L, Lorquet F, Gitton C, van Hylckama Vlieg JET et al. The D-2-hydroxyacid dehydrogenase incorrectly annotated PanE is the sole reduction system for branched-chain 2-keto acids in Lactococcus lactis . J Bacteriol 2009; 191:873–881 [View Article][PubMed]
    [Google Scholar]
  66. Papadimitriou K, Alegría Ángel, Bron PA, de Angelis M, Gobbetti M et al. Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 2016; 80:837–890 [View Article][PubMed]
    [Google Scholar]
  67. Biswas S, Keightley A, Biswas I. Characterization of a stress tolerance-defective mutant of Lactobacillus rhamnosus LRB. Mol Oral Microbiol 2019; 34:153–167 [View Article][PubMed]
    [Google Scholar]
  68. Fontana A, Falasconi I, Molinari P, Treu L, Basile A et al. Genomic comparison of Lactobacillus helveticus strains highlights probiotic potential. Front Microbiol 2019; 10:1380 [View Article][PubMed]
    [Google Scholar]
  69. Daranas N, Badosa E, Francés J, Montesinos E, Bonaterra A. Enhancing water stress tolerance improves fitness in biological control strains of Lactobacillus plantarum in plant environments. In Jogaiah S. editor PLoS One 13(1) 2018 p e0190931
    [Google Scholar]
  70. Jia FF, Zheng HQ, Sun SR, Pang XH, Liang Y et al. Role of luxS in Stress Tolerance and Adhesion Ability in Lactobacillus plantarum KLDS1.0391. Biomed Res Int 2018; 2018:
    [Google Scholar]
  71. Lebeer S, Vanderleyden J, De Keersmaecker SCJ. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 2008; 72:728–764 [View Article][PubMed]
    [Google Scholar]
  72. Jänsch A, Korakli M, Vogel RF, Gänzle MG. Glutathione reductase from Lactobacillus sanfranciscensis DSM20451T: contribution to oxygen tolerance and thiol exchange reactions in wheat sourdoughs. Appl Environ Microbiol 2007; 73:4469–4476 [View Article][PubMed]
    [Google Scholar]
  73. Khairnar NP, Joe MH, Misra HS, Lim SY, Kim DH. FrnE, a cadmium-inducible protein in Deinococcus radiodurans, is characterized as a disulfide isomerase chaperone in vitro and for its role in oxidative stress tolerance in vivo. J Bacteriol 2013; 195:2880–2886 [View Article][PubMed]
    [Google Scholar]
  74. Ehira S, Ohmori M. The redox-sensing transcriptional regulator RexT controls expression of thioredoxin A2 in the cyanobacterium Anabaena sp. strain PCC 7120. J Biol Chem 2012; 287:40433–40440 [View Article][PubMed]
    [Google Scholar]
  75. Krüger E, Witt E, Ohlmeier S, Hanschke R, Hecker M. The Clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J Bacteriol 2000; 182:3259–3265 [View Article][PubMed]
    [Google Scholar]
  76. Michel A, Agerer F, Hauck CR, Herrmann M, Ullrich J et al. Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair. J Bacteriol 2006; 188:5783–5796 [View Article][PubMed]
    [Google Scholar]
  77. Russo P, de la Luz Mohedano M, Capozzi V, de Palencia PF, López P et al. Comparative proteomic analysis of Lactobacillus plantarum WCFS1 and ΔctsR mutant strains under physiological and heat stress conditions. Int J Mol Sci 2012; 13:10680–10696 [View Article][PubMed]
    [Google Scholar]
  78. Gury J, Seraut H, Tran NP, Barthelmebs L, Weidmann S et al. Inactivation of padR, the repressor of the phenolic acid stress response, by molecular interaction with USP1, a universal stress protein from Lactobacillus plantarum, in Escherichia coli . Appl Environ Microbiol 2009; 75:5273–5283 [View Article][PubMed]
    [Google Scholar]
  79. Stoyanov JV, Mancini S, Lu ZH, Mourlane F, Poulsen KR et al. The stress response protein Gls24 is induced by copper and interacts with the CopZ copper chaperone of Enterococcus hirae . FEMS Microbiol Lett 2010; 302:69–75 [View Article][PubMed]
    [Google Scholar]
  80. Pfeiler EA, Azcarate-Peril MA, Klaenhammer TR. Characterization of a novel bile-inducible operon encoding a two-component regulatory system in Lactobacillus acidophilus . J Bacteriol 2007; 189:4624–4634 [View Article][PubMed]
    [Google Scholar]
  81. Azcarate-Peril MA, Altermann E, Goh YJ, Tallon R, Sanozky-Dawes RB et al. Analysis of the genome sequence of Lactobacillus gasseri ATCC 33323 reveals the molecular basis of an autochthonous intestinal organism. Appl Environ Microbiol 2008; 74:4610–4625 [View Article][PubMed]
    [Google Scholar]
  82. O’Flaherty S, Briner Crawley A, Theriot CM, Barrangou R. The Lactobacillus bile salt hydrolase repertoire reveals niche-specific adaptation. In Ellermeier CD. editor mSphere 3(3) 2018
    [Google Scholar]
  83. Barlow M. What antimicrobial resistance has taught us about horizontal gene transfer. vol. 532, methods in molecular biology. Methods Mol Biol 2009397–411
    [Google Scholar]
  84. Rodrigues da Cunha L, Fortes Ferreira CLL, Durmaz E, Goh YJ, Sanozky-Dawes R et al. Characterization of Lactobacillus gasseri isolates from a breast-fed infant. Gut Microbes 2012; 3:15–24 [View Article][PubMed]
    [Google Scholar]
  85. Kaatz GW, McAleese F, Seo SM. Multidrug resistance in Staphylococcus aureus due to overexpression of a novel multidrug and toxin extrusion (MATE) transport protein. Antimicrob Agents Chemother 2005; 49:1857–1864 [View Article][PubMed]
    [Google Scholar]
  86. Campedelli I, Mathur H, Salvetti E, Clarke S, Rea MC et al. Genus-wide assessment of antibiotic resistance in Lactobacillus spp. Appl Environ Microbiol 2019; 85: [View Article][PubMed]
    [Google Scholar]
  87. Wang N, Hang X, Zhang M, Liu X, Yang H. Analysis of newly detected tetracycline resistance genes and their flanking sequences in human intestinal bifidobacteria. Sci Rep 2017; 7:6267 [View Article][PubMed]
    [Google Scholar]
  88. Rozman V, Mohar Lorbeg P, Accetto T, Bogovič Matijašić B. Characterization of antimicrobial resistance in lactobacilli and bifidobacteria used as probiotics or starter cultures based on integration of phenotypic and in silico data. Int J Food Microbiol 2020; 314:108388 [View Article][PubMed]
    [Google Scholar]
  89. Chen J, Li J, Zhang H, Shi W, Liu Y. Bacterial heavy-metal and antibiotic resistance genes in a copper tailing dam area in northern China. Front Microbiol 2019; 10:1–12
    [Google Scholar]
  90. Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DGJ. Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 2015; 16:1–14
    [Google Scholar]
  91. de Jong A, van Hijum SAFT, Bijlsma JJE, Kok J, Kuipers OP. BAGEL: a web-based bacteriocin genome mining tool. Nucleic Acids Res 2006; 34:W273-9W279 [View Article][PubMed]
    [Google Scholar]
  92. Collins FWJ, O’Connor PM, O’Sullivan O, Gómez-Sala B, Rea MC et al. Bacteriocin gene-trait matching across the complete Lactobacillus pan-genome. Sci Rep 2017; 7:1–14
    [Google Scholar]
  93. Collins FWJ, Mesa-Pereira B, O’Connor PM, Rea MC, Hill C et al. Reincarnation of Bacteriocins From the Lactobacillus Pangenomic Graveyard. Front Microbiol 2018; 9:1298 [View Article][PubMed]
    [Google Scholar]
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