Journal Article

Colonocyte metabolism shapes the gut microbiota

Litvak, Yael, Bäumler, Andreas J., Byndloss, Mariana X.

2018

Overview

The gut microbiota affects human health, but we are only just beginning to develop a mechanistic understanding of some of the host-microbe interactions involved. Litvak et al. review how host colon epithelial cells mediate the symbiosis. Healthy colonocytes maintain anaerobic conditions in the gut lumen because their metabolism ensures rapid oxygen consumption. Such conditions select for obligate anaerobic organisms. These tend to be those that consume dietary fiber and produce short-chain fatty acids beneficial to the host. If there is a shift in colonocyte metabolism—because of disease, diet, or other damage—the epithelium becomes oxygenated. The presence of oxygen allows expansion of facultative aerobic organisms. Microbes in genera that include pathogens are often oxygen-tolerant, and dysbiosis can be the result. Science , this issue p. eaat9076 An imbalance in the colonic microbiota might underlie many human diseases, but the mechanisms that maintain homeostasis remain elusive. Recent insights suggest that colonocyte metabolism functions as a control switch, mediating a shift between homeostatic and dysbiotic communities. During homeostasis, colonocyte metabolism is directed toward oxidative phosphorylation, resulting in high epithelial oxygen consumption. The consequent epithelial hypoxia helps to maintain a microbial community dominated by obligate anaerobic bacteria, which provide benefit by converting fiber into fermentation products absorbed by the host. Conditions that alter the metabolism of the colonic epithelium increase epithelial oxygenation, thereby driving an expansion of facultative anaerobic bacteria, a hallmark of dysbiosis in the colon. Enteric pathogens subvert colonocyte metabolism to escape niche protection conferred by the gut microbiota. The reverse strategy, a metabolic reprogramming to restore colonocyte hypoxia, represents a promising new therapeutic approach for rebalancing the colonic microbiota in a broad spectrum of human diseases.

• Publisher: The American Association for the Advancement of Science
• Subject: Anaerobes / Anaerobic bacteria / Anaerobic conditions / Anaerobic microorganisms / Bacteria / Cell Polarity / Coevolution / Colitis, Ulcerative - metabolism / Colitis, Ulcerative - microbiology / Colon / Colon - cytology / Colon - microbiology / Communities / Community Relations / Diet / Dietary fiber / Diseases / Dysbacteriosis / Dysbiosis - metabolism / Dysbiosis - microbiology / Epithelial cells / Epithelium / Fatty acids / Fermentation / Gastrointestinal Microbiome / Homeostasis / Host-Pathogen Interactions / Humans / Hypoxia / Immune system / Intestinal microflora / Intestinal Mucosa - metabolism / Intestine / Lipids / Macrophages / Metabolism / Microbial activity / Microbiota / Microorganisms / Mucosa / Niches / Oxidation / Oxidative phosphorylation / Oxygen / Oxygen Consumption / Oxygenation / Pathogens / Phenotypes / Phosphorylation / Symbiosis / Virulence