Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: Effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties

被引:140
作者
Aoudia, Nabil [1 ]
Rieu, Aurelie [1 ]
Briandet, Romain [2 ,3 ]
Deschamps, Julien [2 ,3 ]
Chluba, Johanna [4 ,5 ,6 ]
Jego, Gaetan [4 ,5 ,6 ]
Garrido, Carmen [4 ,5 ,6 ,7 ]
Guzzo, Jean [1 ]
机构
[1] Univ Bourgogne, AgroSup Dijon, Equipe Vin Alimentat Microbiol Stress, UMR A PAM, F-21000 Dijon, France
[2] INRA, UMR1319 Micalis, F-78352 Jouy En Josas, France
[3] AgroParisTech, UMR Micalis, F-91300 Massy, France
[4] INSERM, UMR 866, Equipe Labellisee Ligue Canc, F-21000 Dijon, France
[5] Lab Excellence LipSTIC, F-21000 Dijon, France
[6] Univ Burgundy, Fac Med & Pharm, F-21000 Dijon, France
[7] Ctr Anticanc George Francois Leclerc CGFL, F-21000 Dijon, France
关键词
Lactobacillus biofilms; Probiotic; Immunomodulatory effects; Zebrafish model; LACTIC-ACID BACTERIA; BILE-SALT HYDROLASE; PROBIOTIC BACTERIA; ESCHERICHIA-COLI; RESISTANCE; COMMUNITIES; ADAPTATION; EXPRESSION; ADHESION; MUCUS;
D O I
10.1016/j.fm.2015.04.009
中图分类号
Q81 [生物工程学(生物技术)]; Q93 [微生物学];
学科分类号
071005 ; 0836 ; 090102 ; 100705 ;
摘要
Few studies have extensively investigated probiotic functions associated with biofilms. Here, we show that strains of Lactobacillus plantarum and Lactobacillus fermentum are able to grow as biofilm on abiotic surfaces, but the biomass density differs between strains. We performed microtiter plate biofilm assays under growth conditions mimicking to the gastrointestinal environment. Osmolarity and low concentrations of bile significantly enhanced Lactobacillus spatial organization. Two L. plantarum strains were able to form biofilms under high concentrations of bile and mucus. We used the agar well-diffusion method to show that supernatants from all Lactobacillus except the NA4 isolate produced food pathogen inhibitory molecules in biofilm. Moreover, TNF-alpha production by LPS-activated human monocytoid cells was suppressed by supernatants from Lactobacillus cultivated as biofilms but not by planktonic culture supernatants. However, only L. fermentum NA4 showed anti-inflammatory effects in zebrafish embryos fed with probiotic bacteria, as assessed by cytokine transcript level (TNF-alpha, IL-1 beta and IL-10). We conclude that the biofilm mode of life is associated with beneficial probiotic properties of lactobacilli, in a strain dependent manner. Those results suggest that characterization of isolate phenotype in the biofilm state could be additional valuable information for the selection of probiotic strains. (C) 2015 Elsevier Ltd. All rights reserved.
引用
收藏
页码:51 / 59
页数:9
相关论文
共 51 条
[1]   Bile stimulates cell surface hydrophobicity, Congo red binding and biofilm formation of Lactobacillus strains [J].
Ambalam, Padma ;
Kondepudi, Kanthi Kiran ;
Nilsson, Ingrid ;
Wadstrom, Torkel ;
Ljungh, Asa .
FEMS MICROBIOLOGY LETTERS, 2012, 333 (01) :10-19
[2]  
[Anonymous], 2001, HLTH NUTR PROP PROB
[3]   The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo [J].
Atuma, C ;
Strugala, V ;
Allen, A ;
Holm, L .
AMERICAN JOURNAL OF PHYSIOLOGY-GASTROINTESTINAL AND LIVER PHYSIOLOGY, 2001, 280 (05) :G922-G929
[4]   Adherence and Cytokine Induction in Caco-2 Cells by Bacterial Populations from a Three-Stage Continuous-Culture Model of the Large Intestine [J].
Bahrami, Bahram ;
Child, Matthew W. ;
Macfarlane, Sandra ;
Macfarlane, George T. .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2011, 77 (09) :2934-2942
[5]   Bile salt hydrolase activity in probiotics [J].
Begley, M ;
Hill, C ;
Gahan, CGM .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2006, 72 (03) :1729-1738
[6]   PROPERTIES OF GASTRIC AND DUODENAL MUCUS - EFFECT OF PROTEOLYSIS, DISULFIDE REDUCTION, BILE, ACID, ETHANOL, AND HYPERTONICITY ON MUCUS GEL STRUCTURE [J].
BELL, AE ;
SELLERS, LA ;
ALLEN, A ;
CUNLIFFE, WJ ;
MORRIS, ER ;
ROSSMURPHY, SB .
GASTROENTEROLOGY, 1985, 88 (01) :269-280
[7]  
Bollinger RR, 2007, GUT, V56, P1481
[8]   The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method [J].
Bridier, A. ;
Dubois-Brissonnet, F. ;
Boubetra, A. ;
Thomas, V. ;
Briandet, R. .
JOURNAL OF MICROBIOLOGICAL METHODS, 2010, 82 (01) :64-70
[9]   Bacterial biofilms: A common cause of persistent infections [J].
Costerton, JW ;
Stewart, PS ;
Greenberg, EP .
SCIENCE, 1999, 284 (5418) :1318-1322
[10]   Selecting lactic acid bacteria for their safety and functionality by use of a mouse colitis model [J].
Daniel, Catherine ;
Poiret, Sabine ;
Goudercourt, Denise ;
Dennin, Veronique ;
Leyer, Gregory ;
Pot, Bruno .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2006, 72 (09) :5799-5805