Abstract
Here, we have analysed and explored the genome sequences of three newly isolated bacteria that were recently characterised for their probiotic activities and ability to produce bacteriocins. These strains, isolated from faeces of animals living in captivity at the zoological garden of Lille (France), are Escherichia coli ICVB443, Enterococcus faecalis ICVB501 and Pediococcus pentosaceus ICVB491. Their genomes have been analysed and compared to those of their pathogenic or probiotic counterparts. The genome analyses of E. coli ICVB443 and Ent. faecalis ICVB501 displayed similarities to those of probiotics E. coli 1917 Nissle, and Ent. faecalis Symbioflor 1, respectively. Furthermore, E. coli ICVB443 shares at least 89 genes with the enteroaggregative E. coli 55989 (EAEC), and Ent. faecalis ICVB501 shares at least 315 genes with the pathogenic Ent. faecalis V583 strain. Unlike Ped. pentosaceus ICVB491, which is devoid of virulence genes, E. coli ICVB443 and Ent. faecalis ICVB501 both carry genes encoding virulence factors on their genomes. Of note, the bioinformatics analysis of these two genomes located the bsh gene, which codes for bile salt hydrolase (BSH). The presence of BSH is of major importance, as it can help to increase the viability of these two strains in the gastrointestinal tract (GIT). The genome analysis of Ped. pentosaceus ICVB491 confirmed its GRAS status (Generally Recognised As Safe), as no genomic virulence factor determinant was found.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Al Seraih A, Belguesmia Y, Cudennec B et al (2018) In silico and experimental data claiming safety aspects and beneficial attributes of the bacteriocinogenic strain enterococcus faecalis B3A-B3B. Probiotics Antimicrob Proteins 10:456–465. https://doi.org/10.1007/s12602-017-9357-8
Aziz RK, Bartels D, Best AA et al (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Baños A, Ariza JJ, Nuñez C et al (2019) Effects of Enterococcus faecalis UGRA10 and the enterocin AS-48 against the fish pathogen Lactococcus garvieae. Studies in vitro and in vivo. Food Microbiol 77:69–77. https://doi.org/10.1016/j.fm.2018.08.002
Belguesmia Y, Domenger D, Caron J et al (2016) Novel probiotic evidence of lactobacilli on immunomodulation and regulation of satiety hormones release in intestinal cells. J Funct Foods 24:276–286. https://doi.org/10.1016/j.jff.2016.04.014
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Borges S, Teixeira P (2014) Pediococcus pentosaceus SB83 as a potential probiotic incorporated in a liquid system for vaginal delivery. Benef Microbes 5:421–426. https://doi.org/10.3920/BM2013.0084
Cebrián R, Baños A, Valdivia E et al (2012) Characterization of functional, safety, and probiotic properties of Enterococcus faecalis UGRA10, a new AS-48-producer strain. Food Microbiol 30:59–67. https://doi.org/10.1016/j.fm.2011.12.002
Corthésy B, Gaskins HR, Mercenier A (2007) Cross-talk between probiotic bacteria and the host immune system. J Nutr 137:781S–790S. https://doi.org/10.1093/jn/137.3.781S
de Man JC, Rogosa M, Sharpe ME (1960) A medium for the cultivation of lactobacilli. J Appl Bacteriol 23:130–135. https://doi.org/10.1111/j.1365-2672.1960.tb00188.x
Domann E, Hain T, Ghai R et al (2007) Comparative genomic analysis for the presence of potential enterococcal virulence factors in the probiotic Enterococcus faecalis strain Symbioflor 1. Int J Med Microbiol 297:533–539. https://doi.org/10.1016/j.ijmm.2007.02.008
Eveno M, Salouhi A, Belguesmia Y et al (2020a) Biodiversity and phylogenetic relationships of novel bacteriocinogenic strains isolated from animal’s droppings at the zoological garden of Lille, France. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-020-09657-4
Eveno M, Savard P, Belguesmia Y, Bazinet L, Gancel F, Drider D, Fliss I (2020b) Compatibility, cytotoxicity, and gastrointestinal tenacity of bacteriocin-producing bacteria selected for a consortium probiotic formulation to be used in livestock feed. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-020-09687-y
FAO/WHO (2002) Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. Guidelines for the Evaluation of Probiotics in Food. https://www.who.int/foodsafety/fs_management/en/probiotic_guidelines.pdf. Accessed 30 Apr 2020
Fijan S (2014) Microorganisms with claimed probiotic properties: an overview of recent literature. Int J Environ Res Public Health 11:4745–4767. https://doi.org/10.3390/ijerph110504745
Gasbarrini G, Bonvicini F, Gramenzi A (2016) Probiotics History. J Clin Gastroenterol 50 Suppl 2, Proceedings from the 8th Probiotics, Prebiotics&New Foods for Microbiota and Human Health meeting held in Rome, Italy on September 13–15, 2015:S116–S119. https://doi.org/10.1097/MCG.0000000000000697
Goldenberg JZ, Lytvyn L, Steurich J et al (2015) Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD004827.pub4
Haakensen M, Vickers DM, Ziola B (2009) Susceptibility of pediococcus isolates to antimicrobial compounds in relation to hop-resistance and beer-spoilage. BMC Microbiol 9:190. https://doi.org/10.1186/1471-2180-9-190
Hardy H, Harris J, Lyon E et al (2013) Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients 5:1869–1912. https://doi.org/10.3390/nu5061869
Jeżewska-Frąckowiak J, Seroczyńska K, Banaszczyk J et al (2018) The promises and risks of probiotic Bacillus species. Acta Biochim Pol 65:509–519. https://doi.org/10.18388/abp.2018_2652
Kafil HS, Mobarez AM, Moghadam MF et al (2016) Gentamicin induces efaA expression and biofilm formation in Enterococcus faecalis. Microb Pathog 92:30–35. https://doi.org/10.1016/j.micpath.2015.12.008
Klare I, Konstabel C, Werner G et al (2007) Antimicrobial susceptibilities of Lactobacillus, Pediococcus and Lactococcus human isolates and cultures intended for probiotic or nutritional use. J Antimicrob Chemother 59:900–912. https://doi.org/10.1093/jac/dkm035
Lebeer S, Vanderleyden J, De Keersmaecker SCJ (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72:728–764. https://doi.org/10.1128/MMBR.00017-08
Ljungh A, Wadström T (2006) Lactic acid bacteria as probiotics. Curr Issues Intest Microbiol 7:73–89
Lukjancenko O, Ussery DW, Wassenaar TM (2012) Comparative genomics of Bifidobacterium, Lactobacillus and related probiotic genera. Microb Ecol 63:651–673. https://doi.org/10.1007/s00248-011-9948-y
Martínez Cruz P, Ibáñez AL, Monroy Hermosillo OA, Ramírez Saad HC (2012) Use of probiotics in aquaculture. ISRN Microbiol 2012:916845. https://doi.org/10.5402/2012/916845
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60
Nueno-Palop C, Narbad A (2011) Probiotic assessment of Enterococcus faecalis CP58 isolated from human gut. Int J Food Microbiol 145:390–394. https://doi.org/10.1016/j.ijfoodmicro.2010.12.029
Ohland CL, Macnaughton WK (2010) Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol Gastrointest Liver Physiol 298:G807–G819. https://doi.org/10.1152/ajpgi.00243.2009
Peralta-Sánchez JM, Martín-Platero AM, Ariza-Romero JJ et al (2019) Egg production in poultry farming is improved by probiotic bacteria. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01042
Sarowska J, Futoma-Koloch B, Jama-Kmiecik A et al (2019) Virulence factors, prevalence and potential transmission of extraintestinal pathogenic Escherichia coli isolated from different sources: recent reports. Gut Pathog 11:10. https://doi.org/10.1186/s13099-019-0290-0
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153
Shepard BD, Gilmore MS (2002) Differential expression of virulence-related genes in Enterococcus faecalis in response to biological cues in serum and urine. Infect Immun 70:4344–4352. https://doi.org/10.1128/IAI.70.8.4344-4352.2002
Stothard P, Wishart DS (2005) Circular genome visualization and exploration using CGView. Bioinformatics 21:537–539. https://doi.org/10.1093/bioinformatics/bti054
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 3:73–79. https://doi.org/10.4161/bbug.18540
Wang J, Tang H, Zhang C et al (2015) Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice. ISME J 9:1–15. https://doi.org/10.1038/ismej.2014.99
Wassenaar TM (2016) Insights from 100 Years of Research with Probiotic E. Coli. Eur J Microbiol Immunol (Bp) 6:147–161. https://doi.org/10.1556/1886.2016.00029
Williams NT (2010) Probiotics. Am J Health Syst Pharm 67:449–458. https://doi.org/10.2146/ajhp090168
Xu L, Dong Z, Fang L et al (2019) OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res 47:W52–W58. https://doi.org/10.1093/nar/gkz333
Yoo JY, Kim SS (2016) Probiotics and prebiotics: present status and future perspectives on metabolic disorders. Nutrients 8:173. https://doi.org/10.3390/nu8030173
Zidour M, Belguesmia Y, Cudennec B et al (2019) Genome sequencing and analysis of Bacillus pumilus ICVB403 isolated from acartia tonsa copepod eggs revealed surfactin and bacteriocin production: insights on anti-staphylococcus activity. Probiotics Antimicrob Proteins 11:990–998. https://doi.org/10.1007/s12602-018-9461-4
Acknowledgements
Mégane Eveno was a recipient of PhD from Lille University (France) and Laval University (Québec, Canada) through the Natural Sciences and Engineering Research Council of Canada (NSERC) METABIOLAC Industrial Research Chair awarded for Prof. Fliss and NSERC Industrial Research Chair on ElectroMembrane processes aiming the ecoefficiency improvement of biofood production lines (Grant IRCPJ 492889-15 to Laurent Bazinet). Research at Lille University was supported by CPER/FEDER Alibiotech programme 2016/2021. The authors are indebted to Dr. S. Elson for critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Eveno, M., Belguesmia, Y., Bazinet, L. et al. In silico analyses of the genomes of three new bacteriocin-producing bacteria isolated from animal’s faeces. Arch Microbiol 203, 205–217 (2021). https://doi.org/10.1007/s00203-020-02016-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-020-02016-5