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A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome.

ABSTRACT: Compartmentalization of the gut microbiota is thought to be important to system function, but the extent of spatial organization in the gut ecosystem remains poorly understood. Here, we profile the murine colonic microbiota along longitudinal and lateral axes using laser capture microdissection. We found fine-scale spatial structuring of the microbiota marked by gradients in composition and diversity along the length of the colon. Privation of fiber reduces the diversity of the microbiota and disrupts longitudinal and lateral gradients in microbiota composition. Both mucus-adjacent and luminal communities are influenced by the absence of dietary fiber, with the loss of a characteristic distal colon microbiota and a reduction in the mucosa-adjacent community, concomitant with depletion of the mucus layer. These results indicate that diet has not only global but also local effects on the composition of the gut microbiota, which may affect function and resilience differently depending on location.

SUBMITTER: Riva A

PROVIDER: S-EPMC6761162 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome.

Riva Alessandra A Kuzyk Orest O Forsberg Erica E Siuzdak Gary G Pfann Carina C Herbold Craig C Daims Holger H Loy Alexander A Warth Benedikt B Berry David D

Nature communications 20190925 1

Compartmentalization of the gut microbiota is thought to be important to system function, but the extent of spatial organization in the gut ecosystem remains poorly understood. Here, we profile the murine colonic microbiota along longitudinal and lateral axes using laser capture microdissection. We found fine-scale spatial structuring of the microbiota marked by gradients in composition and diversity along the length of the colon. Privation of fiber reduces the diversity of the microbiota and di ...[more]

PMID: 31554820

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Project description:BackgroundCognitive impairment, an increasing mental health issue, is a core feature of the aging brain and neurodegenerative diseases. Industrialized nations especially, have experienced a marked decrease in dietary fiber intake, but the potential mechanism linking low fiber intake and cognitive impairment is poorly understood. Emerging research reported that the diversity of gut microbiota in Western populations is significantly reduced. However, it is unknown whether a fiber-deficient diet (which alters gut microbiota) could impair cognition and brain functional elements through the gut-brain axis.ResultsIn this study, a mouse model of long-term (15 weeks) dietary fiber deficiency (FD) was used to mimic a sustained low fiber intake in humans. We found that FD mice showed impaired cognition, including deficits in object location memory, temporal order memory, and the ability to perform daily living activities. The hippocampal synaptic ultrastructure was damaged in FD mice, characterized by widened synaptic clefts and thinned postsynaptic densities. A hippocampal proteomic analysis further identified a deficit of CaMKIId and its associated synaptic proteins (including GAP43 and SV2C) in the FD mice, along with neuroinflammation and microglial engulfment of synapses. The FD mice also exhibited gut microbiota dysbiosis (decreased Bacteroidetes and increased Proteobacteria), which was significantly associated with the cognitive deficits. Of note, a rapid differentiating microbiota change was observed in the mice with a short-term FD diet (7 days) before cognitive impairment, highlighting a possible causal impact of the gut microbiota profile on cognitive outcomes. Moreover, the FD diet compromised the intestinal barrier and reduced short-chain fatty acid (SCFA) production. We exploit these findings for SCFA receptor knockout mice and oral SCFA supplementation that verified SCFA playing a critical role linking the altered gut microbiota and cognitive impairment.ConclusionsThis study, for the first time, reports that a fiber-deprived diet leads to cognitive impairment through altering the gut microbiota-hippocampal axis, which is pathologically distinct from normal brain aging. These findings alert the adverse impact of dietary fiber deficiency on brain function, and highlight an increase in fiber intake as a nutritional strategy to reduce the risk of developing diet-associated cognitive decline and neurodegenerative diseases. Video Abstract.

Project description:Ileocecal resection (ICR) is a commonly required surgical intervention in unmanageable Crohn's disease and necrotizing enterocolitis. However, the impact of ICR, and the concomitant doses of antibiotic routinely given with ICR, on the intestinal commensal microbiota has not been determined. In this study, wild-type C57BL6 mice were subjected to ICR and concomitant single intraperitoneal antibiotic injection. Intestinal lumen contents were collected from jejunum and colon at 7, 14, and 28 days after resection and compared to non-ICR controls. Samples were analyzed by 16S rRNA gene pyrosequencing and quantitative PCR. The intestinal microbiota was altered by 7 days after ICR and accompanying antibiotic treatment, with decreased diversity in the colon. Phylogenetic diversity (PD) decreased from 11.8 ± 1.8 in non-ICR controls to 5.9 ± 0.5 in 7-day post-ICR samples. There were also minor effects in the jejunum where PD values decreased from 8.3 ± 0.4 to 7.5 ± 1.4. PCoA analysis indicated that bacterial populations 28 days post-ICR differed significantly from non-ICR controls. Moreover, colon and jejunum bacterial populations were remarkably similar 28 days after resection, whereas the initial communities differed markedly. Firmicutes and Bacteroidetes were the predominant phyla in jejunum and colon before ICR; however, Firmicutes became the vastly predominant phylum in jejunum and colon 28 days after ICR. Although the microbiota returned towards a homeostatic state, with re-establishment of Firmicutes as the predominant phylum, we did not detect Bacteroidetes in the colon 28 days after ICR. In the jejunum Bacteroidetes was detected at a 0.01% abundance after this time period. The changes in jejunal and colonic microbiota induced by ICR and concomitant antibiotic injection may therefore be considered as potential regulators of post-surgical adaptive growth or function, and in a setting of active IBD, potential contributors to post-surgical pathophysiology of disease recurrence.

Dataset Information

A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome.

Publications

A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome.

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