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, 80 (18), 5782-9

Effect of Lineage-Specific Metabolic Traits of Lactobacillus Reuteri on Sourdough Microbial Ecology

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Effect of Lineage-Specific Metabolic Traits of Lactobacillus Reuteri on Sourdough Microbial Ecology

Xiaoxi B Lin et al. Appl Environ Microbiol.

Abstract

This study determined the effects of specific metabolic traits of Lactobacillus reuteri on its competitiveness in sourdoughs. The competitiveness of lactobacilli in sourdough generally depends on their growth rate; acid resistance additionally contributes to competitiveness in sourdoughs with long fermentation times. Glycerol metabolism via glycerol dehydratase (gupCDE) accelerates growth by the regeneration of reduced cofactors; glutamate metabolism via glutamate decarboxylase (gadB) increases acid resistance by generating a proton motive force. Glycerol and glutamate metabolisms are lineage-specific traits in L. reuteri; therefore, this study employed glycerol dehydratase-positive sourdough isolates of human-adapted L. reuteri lineage I, glutamate decarboxylase-positive strains of rodent-adapted L. reuteri lineage II, as well as mutants with deletions in gadB or gupCDE. The competitivenesses of the strains were quantified by inoculation of wheat and sorghum sourdoughs with defined strains, followed by propagation of doughs with a 10% inoculum and 12-h or 72-h fermentation cycles. Lineage I L. reuteri strains dominated sourdoughs propagated with 12-h fermentation cycles; lineage II L. reuteri strains dominated sourdoughs propagated with 72-h fermentation cycles. L. reuteri 100-23ΔgadB was outcompeted by its wild-type strain in sourdoughs fermented with 72-h fermentation cycles; L. reuteri FUA3400ΔgupCDE was outcompeted by its wild-type strain in sourdoughs fermented with both 12-h and 72-h fermentation cycles. Competition experiments with isogenic pairs of strains resulted in a constant rate of strain displacement of the less competitive mutant strain. In conclusion, lineage-specific traits of L. reuteri determine the competitiveness of this species in sourdough fermentations.

Figures

FIG 1
FIG 1
Microbial compositions of wheat sourdoughs (A and C) and sorghum sourdoughs (B and D) that were inoculated with three L. reuteri strains. Sourdoughs were propagated with 72-h fermentation cycles (A and B) or 12-h fermentation cycles (C and D). Symbols indicate human-lineage L. reuteri FUA3400 (●) and L. reuteri FUA5448 or FUA3168 (○) for cocktail 1 and human-lineage L. reuteri FUA3401 (▼) and L. reuteri FUA5448 or FUA3324 (▽) for cocktail 2. Representative data from two independent experiments are shown.
FIG 2
FIG 2
Growth rates of L. reuteri strains in mMRS broth. White bars indicate glucose as a carbon source (S1 and S2 media), gray bars indicate maltose as a carbon source (W1 and W2 media), and hatched bars indicate the addition of electron acceptors (10 mmol/liter glycerol in S2 medium and 10 mmol/liter sucrose in W2 medium), between S1 and S2 media (*), between W1 and W2 media (**), and between the wild-type strain FUA3400 and the mutant strain FUA3400ΔgupCDE (Δ). Data shown are means ± standard deviations from triplicate independent experiments.
FIG 3
FIG 3
Separation of acetate and 1,3-propanediol in media fermented with L. reuteri FUA3400 or L. reuteri FUA3400ΔgupCDE. Where indicated, media were supplemented with 10 mmol/liter glycerol as an electron acceptor. Chromatograms were offset by 1,500 nRIU (nano-refractive index units).
FIG 4
FIG 4
Growth rates of L. reuteri wild-type strain FUA3400 and L. reuteri mutant strain FUA3400ΔgupCDE in mMRS broth. White bars indicate glucose as a carbon source, matching the major carbon source in sorghum doughs (S1 and S2 media); gray bars indicate maltose as a carbon source, matching the major carbon source in wheat doughs (W1 and W2 media); and hatched bars indicate the addition of electron acceptors (10 mmol/liter glycerol in S2 medium and 10 mmol/liter sucrose in W2 medium). Symbols indicate significant differences (P < 0.05) between S1 and S2 media (*), between W1 and W2 media (**), and between the wild-type strain FUA3400 and the mutant strain FUA3400ΔgupCDE (Δ). Data shown are means ± standard deviations from triplicate independent experiments.
FIG 5
FIG 5
Microbial compositions in sorghum and wheat sourdough fermentations with 12-h and 72-h propagations. Symbols indicate log ratio of L. reuteri FUA3400/L. reuteri FUA3400ΔgupCDE in sorghum (●) and wheat (○) sourdoughs and the log ratio of L. reuteri 100-23/L. reuteri 100-23ΔgadB in sorghum (▼) and wheat (△) sourdoughs. The abundance of L. reuteri FUA3400ΔgupCDE was below the detection limit after 6 propagations. Data shown are means ± standard deviations from triplicate independent experiments.
FIG 6
FIG 6
Concentration of glycerol (black bars) in unfermented wheat, rye, and sorghum sourdoughs and concentration of 1,3-propanediol in wheat, rye, and sorghum sourdoughs after 24 h of fermentation with L. reuteri FUA3400.

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