Context-dependent differences in the functional responses of Lactobacillaceae strains to fermentable sugars

Abstract

Lactobacillaceae are Gram-positive rods, facultative anaerobes, and belong to the lactic acid bacteria (LAB) that frequently serve as probiotics. We systematically compared five LAB strains for the effects of different carbohydrates on their free-living and biofilm lifestyles. We found that fermentable sugars triggered a heterogeneous response in LAB strains, frequently manifested specifically in altered carrying capacity during planktonic growth and colony development. The fermentation capacities of the strains were compatible and could not account for heterogeneity in their differential carrying capacity in liquid and on a solid medium. Among tested LAB strains, L. paracasei, and L. rhamanosus GG survived self-imposed acid stress while L. acidophilus was extremely sensitive to its own glucose utilization acidic products. The addition of a buffering system during growth on a solid medium significantly improved the survival of most tested probiotic strains during fermentation. We suggest that the optimal performance of the beneficial microbiota members belonging to lactobacilli is heterogeneous and varies as a function of the growth model and the dependency on a buffering system.

Metabolic rewiring of the probiotic bacteriumLacticaseibacillus rhamnosusGG contributes to cell-wall remodeling and antimicrobials production

“…While a broad spectrum of pathogenic bacteria are eliminated by LGG in a fermentation-dependent manner (Figure 6), the bacterium itself alters its cell wall (Figure 5C,D,G,H) and biofilm formation (Figure 5E,F), as a potential coping mechanism against the same conditions. Furthermore, our results indicated that cell wall remodeling precedes biofilm formation, and that it is very likely that metabolic rewiring and the accumulation of toxic fermentation products (11) trigger the cell wall remodeling. Also supporting this notion, is that one of the antimicrobial proteins induced during fermentation (Figure 6C) is a D-glutamyl-L-lysyl endopeptidase, targeting peptidoglycan.…”

“…We previously found that fermentable sugars specifically effect the probiotic bacterium LGG, functioning as distinct regulators of growth, aggregation and adhesion (11). The application of glucose, galactose and mannose, which can be fermented by LGG (12) induced growth compared to the tryptic soy broth (TSB) control medium.…”

“…The response of all LAB strains to fermentation is considered uniform and primarily depends on the capacity to utilize glucose and its products (2). However, we recently found that the response of Lacticaseibacillus rhamnosus GG (LGG) to fermentable sugars is strain-specific and includes regulatory responses that are independent of cell growth (11). Glucose utilization has a general role in shaping the colony morphology under static conditions, as all species exhibit morphological colony changes upon glucose treatment (11).…”

“…Glucose utilization has a general role in shaping the colony morphology under static conditions, as all species exhibit morphological colony changes upon glucose treatment (11). Interestingly, buffering of the media restores glucose-free morphology of all strains, indicating that acid stress is involved in biofilm formation throughout the Firmicutes phylum directly or indirectly (11). Glucose-induced change in colony morphology occurred independently of cell death and fermentation-associated pH drop.…”

“…However, we recently found that the response of Lacticaseibacillus rhamnosus GG (LGG) to fermentable sugars is strain-specific and includes regulatory responses that are independent of cell growth (11). Glucose utilization has a general role in shaping the colony morphology under static conditions, as all species exhibit morphological colony changes upon glucose treatment (11). Interestingly, buffering of the media restores glucose-free morphology of all strains, indicating that acid stress is involved in biofilm formation throughout the Firmicutes phylum directly or indirectly (11).…”