Strain-Specific Features of Extracellular Polysaccharides and Their Impact on Lactobacillus plantarum-Host Interactions

• Published in: Applied and environmental microbiology Vol. 82; no. 13; pp. 3959 - 3970
• Main Authors: Lee, I-Chiao, Caggianiello, Graziano, van Swam, Iris I, Taverne, Nico, Meijerink, Marjolein, Bron, Peter A, Spano, Giuseppe, Kleerebezem, Michiel
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 01.07.2016
• Subjects: Carbohydrates; Cells, Cultured; DNA Mutational Analysis; Experiments; Gastrointestinal Tract - microbiology; Gene Deletion; Genes; Genes, Bacterial; Genetics and Molecular Biology; Gram-positive bacteria; Host Microbe Interactomics; Humans; Immunologic Factors - metabolism; Impact analysis; Lactobacillus; Lactobacillus plantarum; Lactobacillus plantarum - genetics; Lactobacillus plantarum - immunology; Lactobacillus plantarum - metabolism; Lactobacillus plantarum - physiology; Leerstoelgroep Host Microbe Interactomics; Leukocytes, Mononuclear - immunology; Metabolic Networks and Pathways - genetics; Microbial Viability; Polysaccharides, Bacterial - genetics; Polysaccharides, Bacterial - metabolism; Probiotics - metabolism; Signal transduction; VLAG; WIAS
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/AEM.00306-16

Lactobacilli are found in diverse environments and are widely applied as probiotic, health-promoting food supplements. Polysaccharides are ubiquitously present on the cell surface of lactobacilli and are considered to contribute to the species- and strain-specific probiotic effects that are typically observed. Two Lactobacillus plantarum strains, SF2A35B and Lp90, have an obvious ropy phenotype, implying high extracellular polysaccharide (EPS) production levels. In this work, we set out to identify the genes involved in EPS production in these L. plantarum strains and to demonstrate their role in EPS production by gene deletion analysis. A model L. plantarum strain, WCFS1, and its previously constructed derivative that produced reduced levels of EPS were included as reference strains. The constructed EPS-reduced derivatives were analyzed for the abundance and sugar compositions of their EPS, revealing cps2-like gene clusters in SF2A35B and Lp90 responsible for major EPS production. Moreover, these mutant strains were tested for phenotypic characteristics that are of relevance for their capacity to interact with the host epithelium in the intestinal tract, including bacterial surface properties as well as survival under the stress conditions encountered in the gastrointestinal tract (acid and bile stress). In addition, the Toll-like receptor 2 (TLR2) signaling and immunomodulatory capacities of the EPS-negative derivatives and their respective wild-type strains were compared, revealing strain-specific impacts of EPS on the immunomodulatory properties. Taken together, these experiments illustrate the importance of EPS in L. plantarum strains as a strain-specific determinant in host interaction. This study evaluates the role of extracellular polysaccharides that are produced by different strains of Lactobacillus plantarum in the determination of the cell surface properties of these bacteria and their capacity to interact with their environment, including their signaling to human host cells. The results clearly show that the consequences of removal of these polysaccharides are very strain specific, illustrating the diverse and unpredictable roles of these polysaccharides in the environmental interactions of these bacterial strains. In the context of the use of lactobacilli as health-promoting probiotic organisms, this study exemplifies the importance of strain specificity.