Leuconostoc mesenteroides mediates an electrogenic pathway to attenuate the accumulation of abdominal fat mass induced by high fat diet

Abstract

Although several electrogenic bacteria have been identified, the physiological effect of electricity generated by bacteria on host health remains elusive. We found that probiotic Leuconostoc mesenteroides (L. mesenteroides) can metabolize linoleic acid to yield electricity via an intracellular cyclophilin A-dependent pathway. Inhibition of cyclophilin A significantly abolished bacterial electricity and lowered the adhesion of L. mesenteroides to the human gut epithelial cell line. Butyrate from L. mesenteroides in the presence of linoleic acid were detectable and mediated free fatty acid receptor 2 (Ffar2) to reduce the lipid contents in differentiating 3T3-L1 adipocytes. Oral administration of L. mesenteroides plus linoleic acid remarkably reduced high-fat-diet (HFD)-induced formation of 4-hydroxy-2-nonenal (4-HNE), a reactive oxygen species (ROS) biomarker, and decreased abdominal fat mass in mice. The reduction of 4-HNE and abdominal fat mass was reversed when cyclophilin A inhibitor-pretreated bacteria were administered to mice. Our studies present a novel mechanism of reducing abdominal fat mass by electrogenic L. mesenteroides which may yield electrons to enhance colonization and sustain high amounts of butyrate to limit ROS during adipocyte differentiation.

In‐depth multiomic characterization of the effects of obesity in high‐fat diet‐fed mice

“…Additionally, Anaerotruncus and Lachnospiraceae were reported to be enriched in the gut of healthy people on a high SFAs diet [ 34 ], which was consistent with our results. Leuconostoc mesenteroides , mediating an electrogenic pathway to attenuate the accumulation of abdominal fat mass induced by HFD [ 35 ], was enriched in HFD‐fed mice in our study. Streptococcus thermophilus positively correlated with obesity [ 36 ], was enriched in HFD‐fed mice.…”

Lactobacillus plantarum Generate Electricity through Flavin Mononucleotide-Mediated Extracellular Electron Transfer to Upregulate Epithelial Type I Collagen Expression and Thereby Promote Microbial Adhesion to Intestine

“…To quantify the adhesion capability of L. plantarum MA with different treatments, 10 µL of the collected L. plantarum MA was seeded on the MRS agar plates using different dilution factors. After maintenance at 37 °C for 12 h, the in vitro adhesion capability of each group was determined based on the value of the microbial population index (MPI) defined by the logarithm of the CFU (MPI = Log 10 ((CFU + 1)/mL)), as previously reported [ 5 ].…”

“…EET allows electrons to be transported from the microbial cytosol to external conductors such as electrodes and/or minerals, and plays an important role in bacterial physiology including growth [ 3 ], colonization [ 5 ], and fermentation [ 6 ]. For example, it has been reported that both Bacillus cereus DIF1 and Rhodococcus ruber DIF2 can secrete redox mediators such as riboflavin and/or flavin mononucleotide (FMN) to promote their growth [ 7 ].…”

“…Electricity generated from Clostridium cochlearium in mice guts can enhance bacterial growth and fermentation [ 6 ]. Our previous work demonstrated that electricity produced from the Gram-positive lactic acid bacteria Leuconostoc mesenteroides is favorable for bacterial colonization in the intestine [ 5 ]. More electrogenic Gram-positive bacteria such as Enterococcus faecalis , Faecalibacterium prausnitzii and Lactococcus lactis which enable flavin-mediated EET were recently discovered by use of a microbial fuel cell chamber (MFCC) [ 8 , 9 , 10 ].…”