Lactobacillus gastricus BTM 7 prevents intestinal colonization by biofilm forming Cronobacter sakazakii in Caenorhabditis elegans model host.
Antimicrobial activity
Biofilm
Caenorhabditis elegans
Cronobacter sakazakii
Probiotics
Journal
Antonie van Leeuwenhoek
ISSN: 1572-9699
Titre abrégé: Antonie Van Leeuwenhoek
Pays: Netherlands
ID NLM: 0372625
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
24
05
2020
accepted:
19
08
2020
pubmed:
13
9
2020
medline:
17
7
2021
entrez:
12
9
2020
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 32918643
doi: 10.1007/s10482-020-01466-7
pii: 10.1007/s10482-020-01466-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1587-1600Subventions
Organisme : Department of Biotechnology, Ministry of Science and Technology (IN)
ID : BT/PR6119/GBD/27/370/2012
Références
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
doi: 10.1128/AEM.66.5.2001-2005.2000
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
doi: 10.3389/fmicb.2016.00464
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
doi: 10.1111/jfs.12017
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
doi: 10.1016/S2222-1808(14)60307-8
Durai S, Pandian SK, Balamurugan K (2011) Establishment of a Caenorhabditis elegans infection model for Vibrio alginolyticus. J Basic Microbiol 51:243–252
doi: 10.1002/jobm.201000303
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
doi: 10.1371/journal.ppat.1000175
Friedemann M (2009) Epidemiology of invasive neonatal Cronobacter (Enterobactersakazakii) infections. Eur J Clin Microbiol infect dis 28:1297–1304
doi: 10.1007/s10096-009-0779-4
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
doi: 10.3389/fmicb.2018.00595
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
doi: 10.3389/fmicb.2017.02409
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
doi: 10.1128/AEM.72.3.2260-2264.2006
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
doi: 10.1371/journal.ppat.1002453
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
doi: 10.1128/AEM.00704-07
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
doi: 10.1099/ijs.0.032292-0
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
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
doi: 10.1128/IAI.06350-11
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
doi: 10.1038/srep31713
Millet AC, Ewbank JJ (2004) Immunity in Caenorhabditis elegans. Curr Opin Immunol 16:4–9
doi: 10.1016/j.coi.2003.11.005
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
doi: 10.1073/pnas.0604055103
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
doi: 10.3389/fmicb.2015.00058
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
doi: 10.1038/s41598-018-25333-8
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
doi: 10.3201/eid2009.140545
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
doi: 10.1007/s11357-016-9889-y
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
doi: 10.1590/S0101-20612010000400027
Reis JA, Paula AT, Casarotti SN et al (2012) Lactic Acid Bacteria Antimicrobial Compounds: Characteristics and Applications. Food Eng Rev 4:124–140
doi: 10.1007/s12393-012-9051-2
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
doi: 10.1007/s12602-018-9466-z
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
doi: 10.1007/s12602-018-9420-0
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
doi: 10.1016/j.micpath.2018.11.041
Singh N, Patil A, Prabhune A, Goel G (2016) Inhibition of quorum-sensing-mediated biofilm formation in Cronobacter sakazakii strains. Microbiology 162:1708–1714
doi: 10.1099/mic.0.000342
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
doi: 10.1002/jobm.201000377
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
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
doi: 10.1371/journal.pbio.1002141
Woo J, Ahn J (2013) Probiotic-mediated competition, exclusion and displacement in biofilm formation by food-borne pathogens. Lett Appl Microbiol 56:307–313
doi: 10.1111/lam.12051
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
doi: 10.1186/2191-0855-2-48
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
doi: 10.1016/j.foodcont.2018.03.038
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
doi: 10.29252/pbr.3.2.39