TY - JOUR
T1 - Selection of immunobiotic ligilactobacillus salivarius strains from the intestinal tract of wakame-fed pigs
T2 - Functional and genomic studies
AU - Zhou, Binghui
AU - Albarracin, Leonardo
AU - Indo, Yuhki
AU - Arce, Lorena
AU - Masumizu, Yuki
AU - Tomokiyo, Mikado
AU - Islam, Md Aminul
AU - Garcia-Castillo, Valeria
AU - Ikeda-Ohtsubo, Wakako
AU - Nochi, Tomonori
AU - Morita, Hidetoshi
AU - Takahashi, Hideki
AU - Kurata, Shoichiro
AU - Villena, Julio
AU - Kitazawa, Haruki
N1 - Funding Information:
This study was supported by grants from the project of NARO Bio-oriented Technology Research Advancement Institution (research program on the development of innovative technology, No. 01002A), and by a Grant-in-Aid for Scientific Research (A) (19H00965) from the Japan Society for the Promotion of Science (JSPS), and by a Grant from the Association for Research on Lactic Acid Bacteria to HK. This study was also supported by ANPCyT–FONCyT Grant PICT-2016-0410 to JV, and by Tohoku University Research Program ‘Frontier Research in Duo’ (FRiD) to SK., and by Japan Racing Association. This work was also supported by grants for Scientific Research on Innovative Areas from the Ministry of Education, Culture, Science, Sports, and Technology (MEXT) of Japan (16H06429, 16K21723, and 16H06435) and Grant-in-Aid for Challenging Research (Exploratory, 19K22300) to HT, and by JSPS Core-to-Core Program, A. Advanced Research Networks entitled Establishment of international agricultural immunology research-core for a quantum improvement in food safety. MAI was supported by JSPS (Postdoctoral Fellowship for Foreign Researchers, Program No. 18F18081). MT was supported by Tohoku University Global Hagi Scholarship.
Publisher Copyright:
© 2020 by the authors. Licensee MDPI, Basel, Switzerland.
PY - 2020/11
Y1 - 2020/11
N2 - In this article, Ligilactobacillus salivarius FFIG strains, isolated from the intestinal tract of wakame-fed pigs, are characterized according to their potential probiotic properties. Strains were evaluated by studying their interaction with porcine intestinal epithelial (PIE) cells in terms of their ability to regulate toll-like receptor (TLR)-3- or TLR4-mediated innate immune responses, as well as by assessing their adhesion capabilities to porcine epithelial cells and mucins. These functional studies were complemented with comparative genomic evaluations using the complete genome sequences of porcine L. salivarius strains selected from subgroups that demonstrated different ‘immune’ and ‘adhesion’ phenotypes. We found that their immunomodulatory and adhesion capabilities are a strain-dependent characteristic. Our analysis indicated that the differential immunomodulatory and adhesive activities of FFIG strains would be dependent on the combination of several surface structures acting simultaneously, which include peptidoglycan, exopolysaccharides, lipoteichoic acid, and adhesins. Of note, our results indicate that there is no correlation between the immunomodulatory capacity of the strains with their adhesion ability to mucins and epithelial cells. Therefore, in the selection of strains destined to colonize the intestinal mucosa and modulate the immunity of the host, both properties must be adequately evaluated. Interestingly, we showed that L. salivarius FFIG58 functionally modulated the innate immune responses triggered by TLR3 and TLR4 activation in PIE cells and efficiently adhered to these cells. Moreover, the FFIG58 strain was capable of reducing rotavirus replication in PIE cells. Therefore, L. salivarius FFIG58 is a good candidate for further in vivo studying the protective effect of lactobacilli against intestinal infections in the porcine host. We also reported and analyzed, for the first time, the complete genome of several L. salivarius strains that were isolated from the intestine of pigs after the selective pressure of feeding the animals with wakame. Further genomic analysis could be of value to reveal the metabolic characteristics and potential of the FFIG strains in general and of the FFIG58 strain, in particular, relating to wakame by-products assimilation.
AB - In this article, Ligilactobacillus salivarius FFIG strains, isolated from the intestinal tract of wakame-fed pigs, are characterized according to their potential probiotic properties. Strains were evaluated by studying their interaction with porcine intestinal epithelial (PIE) cells in terms of their ability to regulate toll-like receptor (TLR)-3- or TLR4-mediated innate immune responses, as well as by assessing their adhesion capabilities to porcine epithelial cells and mucins. These functional studies were complemented with comparative genomic evaluations using the complete genome sequences of porcine L. salivarius strains selected from subgroups that demonstrated different ‘immune’ and ‘adhesion’ phenotypes. We found that their immunomodulatory and adhesion capabilities are a strain-dependent characteristic. Our analysis indicated that the differential immunomodulatory and adhesive activities of FFIG strains would be dependent on the combination of several surface structures acting simultaneously, which include peptidoglycan, exopolysaccharides, lipoteichoic acid, and adhesins. Of note, our results indicate that there is no correlation between the immunomodulatory capacity of the strains with their adhesion ability to mucins and epithelial cells. Therefore, in the selection of strains destined to colonize the intestinal mucosa and modulate the immunity of the host, both properties must be adequately evaluated. Interestingly, we showed that L. salivarius FFIG58 functionally modulated the innate immune responses triggered by TLR3 and TLR4 activation in PIE cells and efficiently adhered to these cells. Moreover, the FFIG58 strain was capable of reducing rotavirus replication in PIE cells. Therefore, L. salivarius FFIG58 is a good candidate for further in vivo studying the protective effect of lactobacilli against intestinal infections in the porcine host. We also reported and analyzed, for the first time, the complete genome of several L. salivarius strains that were isolated from the intestine of pigs after the selective pressure of feeding the animals with wakame. Further genomic analysis could be of value to reveal the metabolic characteristics and potential of the FFIG strains in general and of the FFIG58 strain, in particular, relating to wakame by-products assimilation.
KW - Adhesion
KW - Genomics
KW - Immunomodulation
KW - Ligilactobacillus salivarius
KW - Pigs
KW - Porcine intestinal epithelial cells
KW - Wakame
UR - http://www.scopus.com/inward/record.url?scp=85095567609&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85095567609&partnerID=8YFLogxK
U2 - 10.3390/microorganisms8111659
DO - 10.3390/microorganisms8111659
M3 - Article
AN - SCOPUS:85095567609
SN - 2076-2607
VL - 8
SP - 1
EP - 28
JO - Microorganisms
JF - Microorganisms
IS - 11
M1 - 1659
ER -