Dietary metabolites derived from gut microbiota: critical modulators of epigenetic changes in mammals

Abstract

The mammalian gastrointestinal tract harbors trillions of commensal microorganisms, collectively known as the microbiota. The microbiota is a critical source of environmental stimuli and, thus, has a tremendous impact on the health of the host. The microbes within the microbiota regulate homeostasis within the gut, and any alteration in their composition can lead to disorders that include inflammatory bowel disease, allergy, autoimmune disease, diabetes, mental disorders, and cancer. Hence, restoration of the gut flora following changes or imbalance is imperative for the host. The low-molecular-weight compounds and nutrients such as short-chain fatty acids, polyamines, polyphenols, and vitamins produced by microbial metabolism of nondigestible food components in the gut actively participate in various epigenomic mechanisms that reprogram the genome by altering the transcriptional machinery of a cell in response to environmental stimuli. These epigenetic modifications are caused by a set of highly dynamic enzymes, notably histone acetylases, deacetylases, DNA methylases, and demethylases, that are influenced by microbial metabolites and other environmental cues. Recent studies have shown that host expression of histone acetylases and histone deacetylases is important for regulating communication between the intestinal microbiota and the host cells. Histone acetylases and deacetylases influence the molecular expression of genes that affect not only physiological functions but also behavioral shifts that occur via neuroepigenetic modifications of genes. The underlying molecular mechanisms, however, have yet to be fully elucidated and thus provide a new area of research. The present review provides insights into the current understanding of the microbiota and its association with mammalian epigenomics as well as the interaction of pathogens and probiotics with host epigenetic machinery.

Structural and compositional mismatch between captive and wild Atlantic salmon (Salmo salar) parrs’ gut microbiota highlights the relevance of integrating molecular ecology for management and conservation methods

“…It has also been demonstrated that reared fish show a different methylation pattern than that of their wild relatives (Le Luyer et al., ). As energetic and behavioral phenotypes are controlled by gut microbiota activity (Tremaroli & Bäckhed, ) and the latter is suspected to impact epigenetic patterns (Bhat & Kapila, ; Cortese et al., ; Indrio et al., ; Rossi et al., ), our study is of prime interest as it is the first to demonstrate the extensive impact of captive rearing on gut microbiota composition in Atlantic salmon parrs meant for stocking. By identifying significant differences in terms of both structure and taxonomic composition between captive parrs and their wild relatives, the present work evidenced that acclimation to artificial rearing is also observable at the host–microbiota level.…”

“…It has also been observed that gene regulation and hormone secretion of the host are affected by metabolites from bacterial activity acting as signal molecules (Tremaroli & Bäckhed, ). Recent studies have also linked the microbiota composition with modification in epigenetic patterns in newborns, increasing the need to further investigate the role of the microbiota in the understanding of the phenotypic plasticity in teleosts (Bhat & Kapila, ; Cortese, Lu, Yu, Ruden, & Claud, ; Indrio et al., ; Rossi, Amaretti, & Raimondi, ). Because host–microbiota interactions are narrowly related to the host physiology (Donaldson et al., ; Klaasen et al., ; Liu et al., ; Scanlan et al., ; Wu & Lewis, ; Zhang, Lun, & Tsui, ), it is suspected that bacterial composition of microbial communities will tightly adapt to artificial rearing conditions (water composition, food, environmental bacterial community), which in turn will affect the ability of hatchery‐reared parrs to adapt to natural conditions once released.…”

Modulation of Intestinal Epithelial Glycocalyx Development by Human Milk Oligosaccharides and Non‐Digestible Carbohydrates

“…The hMOs and NDCs investigated here do stimulate the development of the glycocalyx on intestinal epithelial cells. This may be a possible mechanism for the observed enhancing effects of hMOs and NDCs and its beneficial effects on gut microbiota that need the glycocalyx to adhere to the gut epithelium, with subsequent positive effects on fermentation products short chain fatty acids (SCFAs) and vitamins . Also, it may be a possible mechanistic explanation for the hMOs and NDCs induced enhanced gut barrier function .…”

Impact of the gut microbiome on the genome and epigenome of colon epithelial cells: contributions to colorectal cancer development

“…The first is the capacity of gut microbes to induce a pro-carcinogenic inflammatory response [41][42][43]. The second is the production of secondary metabolites by gut microbes [44][45][46]. The ability of short chain fatty acids (SCFAs), hydrogen sulfide (H 2 S), secondary bile acids, and many other metabolites to impact the genome or epigenome of CECs, to alter rates of CRC progression, and to function as targets for CRC prevention or treatment is tremendously important and has thus been the topic of many recent reviews [47][48][49][50].…”