TY - JOUR
T1 - Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection
AU - Fanning, Saranna
AU - Hall, Lindsay J.
AU - Cronin, Michelle
AU - Zomer, Aldert
AU - MacSharry, John
AU - Goulding, David
AU - Motherway, Mary O.Connell
AU - Shanahan, Fergus
AU - Nally, Kenneth
AU - Dougan, Gordon
AU - Van Sinderen, Douwe
PY - 2012/2/7
Y1 - 2012/2/7
N2 - Bifidobacteria comprise a significant proportion of the human gut microbiota. Several bifidobacterial strains are currently used as therapeutic interventions, claiming various health benefits by acting as probiotics. However, the precise mechanisms by which they maintain habitation within their host and consequently provide these benefits are not fully understood. Here we show that Bifidobacterium breve UCC2003 produces a cell surface-associated exopolysaccharide (EPS), the biosynthesis ofwhich is directed by either half of a bidirectional gene cluster, thus leading to production of one of two possible EPSs.Alternate transcription of the two opposinghalves of this cluster appears to be the result of promoter reorientation. Surface EPS provided stress tolerance and promoted in vivo persistence, but not initial colonization. Marked differences were observed in host immune response: strains producing surface EPS (EPS +) failed to elicit a strong immune response compared with EPS-deficient variants. Specifically, EPS production was shown to be linked to the evasion of adaptive B-cell responses. Furthermore, presence of EPS + B. breve reduced colonization levels of the gut pathogen Citrobacter rodentium. Our data thus assigns a pivotal and beneficial role for EPS in modulating various aspects of bifidobacterial-host interaction, including the ability of commensal bacteria to remain immunologically silent and in turn provide pathogen protection. This finding enforces the probiotic concept and provides mechanistic insights into health-promoting benefits for both animal and human hosts.
AB - Bifidobacteria comprise a significant proportion of the human gut microbiota. Several bifidobacterial strains are currently used as therapeutic interventions, claiming various health benefits by acting as probiotics. However, the precise mechanisms by which they maintain habitation within their host and consequently provide these benefits are not fully understood. Here we show that Bifidobacterium breve UCC2003 produces a cell surface-associated exopolysaccharide (EPS), the biosynthesis ofwhich is directed by either half of a bidirectional gene cluster, thus leading to production of one of two possible EPSs.Alternate transcription of the two opposinghalves of this cluster appears to be the result of promoter reorientation. Surface EPS provided stress tolerance and promoted in vivo persistence, but not initial colonization. Marked differences were observed in host immune response: strains producing surface EPS (EPS +) failed to elicit a strong immune response compared with EPS-deficient variants. Specifically, EPS production was shown to be linked to the evasion of adaptive B-cell responses. Furthermore, presence of EPS + B. breve reduced colonization levels of the gut pathogen Citrobacter rodentium. Our data thus assigns a pivotal and beneficial role for EPS in modulating various aspects of bifidobacterial-host interaction, including the ability of commensal bacteria to remain immunologically silent and in turn provide pathogen protection. This finding enforces the probiotic concept and provides mechanistic insights into health-promoting benefits for both animal and human hosts.
UR - http://www.scopus.com/inward/record.url?scp=84857128238&partnerID=8YFLogxK
U2 - 10.1073/pnas.1115621109
DO - 10.1073/pnas.1115621109
M3 - Article
C2 - 22308390
AN - SCOPUS:84857128238
SN - 0027-8424
VL - 109
SP - 2108
EP - 2113
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 6
ER -