Abstract
Over the past century, soybean oil (SBO) consumption in the United States increased dramatically. The main SBO fatty acid, linoleic acid (18:2), inhibits in vitro the growth of lactobacilli, beneficial members of the small intestinal microbiota. Human-associated lactobacilli have declined in prevalence in Western microbiomes, but how dietary changes may have impacted their ecology is unclear. Here, we compared the in vitro and in vivo effects of 18:2 on Lactobacillus reuteri and L. johnsonii. Directed evolution in vitro in both species led to strong 18:2 resistance with mutations in genes for lipid biosynthesis, acid stress, and the cell membrane or wall. Small-intestinal Lactobacillus populations in mice were unaffected by chronic and acute 18:2 exposure, yet harbored both 18:2- sensitive and resistant strains. This work shows that extant small intestinal lactobacilli are protected from toxic dietary components via the gut environment as well as their own capacity to evolve resistance.
Highlights
While antibiotics can cause lasting alterations to the microbiome (David et al, 2014a; Dethlefsen et al, 2008; Dethlefsen and Relman, 2011; Jakobsson et al, 2010), dietary perturbations rarely do so (Sonnenburg et al, 2016)
We confirmed the previously reported in vitro toxicity of long chain fatty acids (FAs) towards L. reuteri by performing disc diffusion assays with the individual free FAs of soybean oil (SBO) using L. reuteri ATCC 53608
This inhibitory concentration 50 (IC50) concurs with our estimates of the concentration of 18:2 present in a mouse consuming a SBO diet (11 to 28 mg/ml for a mouse on a 7% by weight SBO diet, see Materials and methods) and with previous estimates of mammalian physiological relevant concentrations of unsaturated FAs (Kankaanpaaet al., 2001; Kodicek, 1945)
Summary
While antibiotics can cause lasting alterations to the microbiome (David et al, 2014a; Dethlefsen et al, 2008; Dethlefsen and Relman, 2011; Jakobsson et al, 2010), dietary perturbations rarely do so (Sonnenburg et al, 2016). Among the microbes inhibited by linoleic acid is a beneficial bacterium called Lactobacillus reuteri This microbe has become less common in Western populations, and the timing of its decline approximately follows when the consumption of soybean oil began increasing. L. reuteri and other related microbes still exist in people who eat a Western diet This suggests that these bacteria must be protected from linoleic acid in the gut, or that they can become resistant to this toxic molecule. The resistant bacteria recovered from the mice did not have mutations in the genes that had been identified from the earlier experiments Together these findings show that gut bacteria have several means of surviving the high levels of potentially toxic fat molecules. Lactobacilli populations were quantified in live-only and whole cell fractions obtained from the small intestine, and isolates from mice were assessed for resistance in vitro
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