Abstract
Microvesicles are small lipid, bilayer structures (20–400 nm in diameter) secreted by bacteria, fungi, archaea and parasites involved in inter-bacterial communication and host-pathogen interactions. Lactobacillus reuteri DSM-17938 (DSM) has been shown to have clinical efficacy in the treatment of infantile colic, diarrhea and constipation. We have shown previously that luminal administration to the mouse gut promotes reduction of jejunal motility but increases that in the colon. The production of microvesicles by DSM has been characterized, but the effect of these microvesicles on gastrointestinal motility has yet to be evaluated. To investigate a potential mechanism for the effects of DSM on the intestine, the bacteria and its products have here been tested for changes in velocity, frequency, and amplitude of contractions in intact segments of jejunum and colon excised from mice. The effect of the parent bacteria (DSM) was compared to the conditioned media in which it was grown, and the microvesicles it produced. The media used to culture the bacteria (broth) was tested as a negative control and the conditioned medium was tested after the microvesicles had been removed. DSM, conditioned medium, and the microvesicles all produced comparable effects in both the jejunum and the colon. The treatments individually decreased the velocity and frequency of propagating contractile cluster contractions in the jejunum and increased them in the colon to a similar degree. The broth control had little effect in both tissues. Removal of the microvesicles from the conditioned medium almost completely eradicated their effect on motility in both tissues. These results show that the microvesicles from DSM alone can completely reproduce the effects of the whole bacteria on gut motility. Furthermore, they suggest a new approach to the formulation of orally active bacterial therapeutics and offer a novel way to begin to identify the active bacterial components.
Highlights
Eukaryotic and prokaryotic microorganisms including bacteria, archaea, fungi, and parasites all produce and release spherical membrane vesicles referred to throughout the literature by such names as outer membrane vesicles (OMV), exosomes or microvesicles, depending on their origin [1]
We isolated the μV from conditioned media in which DSM bacteria were grown, in order to compare their effect on GI motility to that of the parent bacteria. We compared these activities to those of the conditioned media in which bacteria had been removed and the effects of the medium alone. In these experiments we have shown clearly that bacterial μV may represent a major pathway through which DSM exerts its effects on gut motility
The growth media used to culture the bacteria was applied separately. The effect of these treatments was compared to Krebs buffer control and measured across three parameters of propagating contractile complexes (PCC) in the gut segments: velocity, frequency, and amplitude (Fig 1C)
Summary
Eukaryotic and prokaryotic microorganisms including bacteria, archaea, fungi, and parasites all produce and release spherical membrane vesicles referred to throughout the literature by such names as outer membrane vesicles (OMV), exosomes or microvesicles, depending on their origin [1]. Bacterial membrane vesicles, referred to in this paper as microvesicles (μV), are small spherical structures (20–400 nm) that bleb from the membrane of both Gram-negative and Gram-positive bacteria [2] They may contain macromolecules as varied as phospholipids, proteins, lipopolysaccharides, peptidoglycans, carbohydrates and nucleic acids [3,4]. We have demonstrated previously that the μV from a beneficial Gram-positive bacteria, L, rhamnosus JB-1 (JB-1), reproduced the immune and neuronal functional activities of JB-1, in vivo, ex vivo and in vitro [9] These studies convincingly show that bacterial μV may have important properties in terms of gut bacteria-host communication and are at least one pathway whereby bacteria may regulate host physiology
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