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Lactobacillus gastricus BTM 7 prevents intestinal colonization by biofilm forming Cronobacter sakazakii in Caenorhabditis elegans model host

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Abstract

The study reports protective role of potential probiotic cultures against infection by biofilm forming Cronobacter sakazakii in Caenorhabditis elegans model system. Among the fifteen indigenous potential probiotics, the cell free supernatant of Lactobacillus gastricus BTM7 possessed highest antimicrobial action and biofilm inhibition against C. sakazakii. The competitive exclusion assays revealed that preconditioning with probiotics resulted in increased mean life span of the nematode to 12–13 days as compared to 5–6 days when the pathogen was administered alone. Enhanced expression of the marker genes (pmk-1, daf-16 and skn-1) was observed during the administration of probiotic cultures. The highest expression of pmk-1 (2.5 folds) was observed with administration of L. gastricus BTM7. The principal component analysis on selected variables revealed that L. gastricus BTM7 has the potential to limit the infection of C. sakazakii in C. elegans and enhance the expression of key genes involved in extending life span of the worm.

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References

  • Alakomi HL, Skyttä E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM (2000) Lactic acid permeabilizes gram-negative bacteria by disrupting the outer membrane. Appl Environ Microbiol 66:2001–2005

    Article  CAS  Google Scholar 

  • Arena MP, Silvain A, Normanno G, Grieco F, Drider D, Spano G, Fiocco D (2016) Use of Lactobacillus plantarum strains as a biocontrol strategy against food-borne pathogenic microorganisms. Front Microbiol 7:464

    Article  Google Scholar 

  • Ben Slama R, Kouidhi B, Zmantar T, Chaieb K, Bakhrouf A (2013) Anti-listerial and Anti-biofilm Activities of Potential Probiotic Lactobacillus Strains Isolated from Tunisian Traditional Fermented Food. J Food Saf 33:8–16

    Article  Google Scholar 

  • Dasari S, Shouri RND, Wudayagiri R, Valluru L (2014) Antimicrobial activity of Lactobacillus against microbial flora of cervicovaginal infections. Asian Pac J Trop Dis 4:18

    Article  Google Scholar 

  • Durai S, Pandian SK, Balamurugan K (2011) Establishment of a Caenorhabditis elegans infection model for Vibrio alginolyticus. J Basic Microbiol 51:243–252

    Article  CAS  Google Scholar 

  • Evans EA, Kawli T, Tan MW (2008) Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans. PLoS Pathog 4:e1000175

    Article  Google Scholar 

  • Friedemann M (2009) Epidemiology of invasive neonatal Cronobacter (Enterobactersakazakii) infections. Eur J Clin Microbiol infect dis 28:1297–1304

    Article  CAS  Google Scholar 

  • Guantario B, Zinno P, Schifano E, Roselli M, Perozzi G, Palleschi C, Uccelletti D, Devirgiliis C (2018) In vitro and in vivo selection of potentially probiotic lactobacilli from Nocellara del Belice table olives. Front Microbiol 9:595

    Article  Google Scholar 

  • Grassi L, Maisetta G, Esin S, Batoni G (2017) Combination strategies to enhance the efficacy of antimicrobial peptides against bacterial biofilms. Front Microbiol 8:2409

    Article  Google Scholar 

  • Hayes M, Ross RP, Fitzgerald GF, Hill C, Stanton C (2006) Casein-derived antimicrobial peptides generated by Lactobacillus acidophilus DPC6026. Appl Environ Microbiol 72:2260–2264

    Article  CAS  Google Scholar 

  • Hoeven R, McCallum KC, Cruz MR, Garsin DA (2011) Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog 7:e1002453

    Article  Google Scholar 

  • Ikeda T, Yasui C, Hoshino K, Arikawa K, Nishikawa Y (2007) Influence of lactic acid bacteria on longevity of Caenorhabditis elegans and host defense against Salmonella enterica serovar enteritidis. Appl Environ Microbiol 73:6404–6409

    Article  CAS  Google Scholar 

  • Joseph S, Cetinkaya E, Drahovska H, Levican A, Figueras MJ, Forsythe SJ (2012) Cronobacter condimenti sp. nov., isolated from spiced meat, and Cronobacter universalis sp. nov., a species designation for Cronobacter sp. genomospecies 1, recovered from a leg infection, water, and food ingredients. Int J Syst Evol Microbiol 62:1277–1283

    Article  CAS  Google Scholar 

  • Kamladevi A, Balamurugan K (2015) Role of PMK-1/p38 MAPK defense in Caenorhabditis elegans against Klebsiella pneumoniae infection during host-pathogen interaction. Pathog Dis 73:ftv021

    Google Scholar 

  • Kim Y, Mylonakis E (2012) Caenorhabditis elegans immune conditioning with the probiotic bacterium Lactobacillus acidophilus NCFM enhances gram-positive immune responses. Infect Immun 80:2500–2508

    Article  CAS  Google Scholar 

  • Kwon G, Lee J, Lim JH (2016) Dairy Propionibacterium extends the mean lifespan of Caenorhabditis elegans via activation of the innate immune system. Sci Rep 6:31713

    Article  CAS  Google Scholar 

  • Millet AC, Ewbank JJ (2004) Immunity in Caenorhabditis elegans. Curr Opin Immunol 16:4–9

    Article  CAS  Google Scholar 

  • Moy TI, Ball AR, Anklesaria Z, Casadei G, Lewis K, Ausubel FM (2006) Identification of novel antimicrobials using a live-animal infection model. Proc Natl Acad Sci 103:10414–10419

    Article  CAS  Google Scholar 

  • Papadimitriou K, Zoumpopoulou G, Foligné B, Alexandraki V, Kazou M, Pot B, Tsakalidou E (2015) Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front Microbiol 6:58

    Article  Google Scholar 

  • Park MR, Ryu S, Maburutse BE, Oh NS, Kim SH, Oh S, Jeong SY, Jeong DY (2018) Probiotic Lactobacillus fermentum strain JDFM216 stimulates the longevity and immune response of Caenorhabditis elegans through a nuclear hormone receptor. Sci Rep 8:7441

    Article  Google Scholar 

  • Patrick ME, Mahon BE, Greene SA, Rounds J, Cronquist A, Wymore K et al (2014) Incidence of Cronobacter spp. infections, United States, 2003–2009. Emerg Infect Dis 20:1520

    Article  Google Scholar 

  • Prasanth MI, Santoshram GS, Bhaskar JP, Balamurugan K (2016) Ultraviolet-a triggers photoaging in model nematode Caenorhabditis elegans in a DAF-16 dependent pathway. Age 38:27

    Article  Google Scholar 

  • Ratti RP, Gomes BC, Martinez RCR, Souza VM, Martinis ECPD (2010) Elongated cells of Listeria monocytogenes in biofilms in the presence of sucrose and bacteriocin-producing Leuconostoc mesenteroides A11. Food Sci Technol (Campinas) 30:1011–1016

    Article  Google Scholar 

  • Reis JA, Paula AT, Casarotti SN et al (2012) Lactic Acid Bacteria Antimicrobial Compounds: Characteristics and Applications. Food Eng Rev 4:124–140

    Article  CAS  Google Scholar 

  • Sharma K, Attri S, Goel G (2019a) Selection and evaluation of probiotic and functional characteristics of autochthonous lactic acid bacteria isolated from fermented wheat flour dough babroo. Probiotics Antimicrob Proteins 11:774–784

    Article  CAS  Google Scholar 

  • Sharma K, Pooranachithra M, Balamurugan K, Goel G (2019b) Multivariate analysis of increase in life span of Caenorhabditis elegans through intestinal colonization by indigenous probiotic strains. Probiotics Antimicrob Proteins 11:865–873

    Article  CAS  Google Scholar 

  • Sharma K, Pooranachithra M, Balamurugan K, Goel G (2019c) Probiotic mediated colonization resistance against E. coli infection in experimentally challenged Caenorhabditis elegans. Microb Pathog 127:39–47

    Article  Google Scholar 

  • Singh N, Patil A, Prabhune A, Goel G (2016) Inhibition of quorum-sensing-mediated biofilm formation in Cronobacter sakazakii strains. Microbiology 162:1708–1714

    Article  CAS  Google Scholar 

  • Sivamaruthi BS, Ganguli A, Kumar M, Bhaviya S, Pandian SK, Balamurugan K (2011) Caenorhabditis elegans as a model for studying Cronobacter sakazakii ATCC BAA-894 pathogenesis. J Basic Microbiol 51:540–549

    Article  CAS  Google Scholar 

  • Tahmourespour A, Salehi R, Kermanshahi RK (2011) Lactobacillus acidophilus-derived biosurfactant effect on gtfB and gtfC expression level in Streptococcus mutans biofilm cells Braz. J Microbiol 42:330–339

    CAS  Google Scholar 

  • Van Gestel J, Vlamakis H, Kolter R (2015) From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate. PLoS Biol 1:e1002141

    Article  Google Scholar 

  • Woo J, Ahn J (2013) Probiotic-mediated competition, exclusion and displacement in biofilm formation by food-borne pathogens. Lett Appl Microbiol 56:307–313

    Article  CAS  Google Scholar 

  • Yang E, Fan L, Jiang Y, Doucette C, Fillmore S (2012) Antimicrobial activity of bacteriocin-producing lactic acid bacteria isolated from cheeses and yogurts. Amb Express 2:48

    Article  Google Scholar 

  • Yi L, Li X, Luo L, Lu Y, Yan H, Qiao Z, Lü X (2018) A novel bacteriocin BMP11 and its antibacterial mechanism on cell envelope of Listeria monocytogenes and Cronobacter sakazakii. Food Control 91:160–169

    Article  CAS  Google Scholar 

  • Zamani H, Rahbar S, Garakoui SR, Afsah Sahebi A, Jafari H (2017) Antibiofilm potential of Lactobacillus plantarum spp. cell free supernatant (CFS) against multidrug resistant bacterial pathogens. Pharma Biomed Res 3:39–44

    Article  CAS  Google Scholar 

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Acknowledgements

The authors wish to thank Department of Biotechnology (DBT), Govt. of India, for providing financial support and Jaypee University of Information Technology for essential facilities required for the research work.

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KS, PM, MIP performed and executed the experiments, KS,NS, KB and GG contributed to text preparation and revised the manuscript. All authors read and approved the final version of the manuscript.

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Correspondence to Gunjan Goel.

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Kavita, S., Pooranachithra, M., Singh, N. et al. Lactobacillus gastricus BTM 7 prevents intestinal colonization by biofilm forming Cronobacter sakazakii in Caenorhabditis elegans model host. Antonie van Leeuwenhoek 113, 1587–1600 (2020). https://doi.org/10.1007/s10482-020-01466-7

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