Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut

Roager, Henrik Munch; Hansen, Lea Benedicte Skov; Bahl, Martin Iain; Frandsen, Henrik Lauritz; Carvalho, Vera; Gøbel, Rikke Juul; Dalgaard, Marlene Danner; Plichta, Damian R.; Sparholt, Morten H.; Vestergaard, Henrik; Hansen, Torben; Sicheritz-Pontén, Thomas; Nielsen, Henrik Bjørn; Pedersen, Oluf; Lauritzen, Lotte; Kristensen, Mette; Gupta, Ramneek; Licht, Tine Rask

doi:10.1038/nmicrobiol.2016.93

Cited by 358 publications

(342 citation statements)

References 67 publications

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“…6, Inset). Furthermore, microbiome sequencing has confirmed nutrient inflow, transit time, and water content to be crucial determinants of microbiota composition (31,32,45,46), with stool consistency (BSS) identified as the single most important factor explaining microbiota variation in a large-scale epidemiological study (44). Our results offer a minimal explanation for these variations: Nutrient inflow and stool consistency affect microbiota composition via changes in luminal pH.…”

Section: Discussionmentioning

confidence: 66%

Effect of water flow and chemical environment on microbiota growth and composition in the human colon

Cremer

Arnoldini

Hwa

2017

Proc. Natl. Acad. Sci. U.S.A.

143

192

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The human gut harbors a dynamic microbial community whose composition bears great importance for the health of the host. Here, we investigate how colonic physiology impacts bacterial growth, which ultimately dictates microbiota composition. Combining measurements of bacterial physiology with analysis of published data on human physiology into a quantitative, comprehensive modeling framework, we show how water flow in the colon, in concert with other physiological factors, determine the abundances of the major bacterial phyla. Mechanistically, our model shows that local pH values in the lumen, which differentially affect the growth of different bacteria, drive changes in microbiota composition. It identifies key factors influencing the delicate regulation of colonic pH, including epithelial water absorption, nutrient inflow, and luminal buffering capacity, and generates testable predictions on their effects. Our findings show that a predictive and mechanistic understanding of microbial ecology in the gut is possible. Such predictive understanding is needed for the rational design of intervention strategies to actively control the microbiota. T he human gut microbiota is composed of trillions of bacterial cells (1-4) from several hundred species (1-3, 5, 6). Over the last two decades, a multitude of studies have shown a strong impact of human health status on the composition of this microbiota, and in turn a strong effect of microbiota composition on host physiology has also been confirmed (7-9). Various intervention strategies are being investigated to modify the microbiota composition via prebiotics and probiotics (10). Despite this importance for human health, little is known about how the microbiota composition is shaped by the interplay between human and bacterial physiology in the gut.In this study, we present a physiological model that quantitatively describes this host-microbiota interplay. Our model is based on a hydrodynamic perspective, which posits that bacterial densities reached in the colon result from a dynamic balance between bacterial growth, flow through the colon, and peristaltic mixing (11). To build the present model, we extensively analyzed literature data on human gut physiology to obtain quantitative estimates for a range of relevant host parameters. We further characterized the rates of bacterial growth, carbohydrate consumption, and fermentation product excretion for representatives of the two dominant bacteria phyla, Bacteroidetes and Firmicutes, that typically make up more than 90% of the bacterial cells observed in the gut (6).Combining these aspects of human and bacterial physiology into a coarse-grained mathematical model allowed us to study bacterial growth dynamics in the human gut. Without resorting to ad hoc fitting parameters, model results are in quantitative agreement with available data on key observables of human gut physiology. We find that changes in pH values in the colon that are due to the secretion of acidic fermentation products and shaped by human physiology (such a...

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Section: Discussionmentioning

confidence: 66%

Effect of water flow and chemical environment on microbiota growth and composition in the human colon

Cremer

Arnoldini

Hwa

2017

Proc. Natl. Acad. Sci. U.S.A.

143

192

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“…The modulating effect of specific growth rate on the colon microbiota is not understood, yet, however, it can be assumed that faster transit supports fast-growing bacteria and vice versa . Roager et al showed that long transit time is associated with higher abundances of Methanobrevibacterium and certain taxa from Ruminococcaceae and Christensenellaceae in adult fecal microbiota [4]. Despite the significance of the transit time, this parameter is difficult to measure in practice.…”

Section: Discussionmentioning

confidence: 99%

“…The fibers that are only partially or non-fermented by the gut microbiota increase the fecal volume and transit rate by binding to water. Peristalsis, water absorption, environmental acidity, redox potential, and the absorption of nutrients are affected by the intestinal microbiota, and in turn, affect the microbiota as well [3,4]. Hence, short bowel transit time (below 24 h) might support the fast-growing bacteria and can be a key factor to control the fermentation of dietary fibers in the colon.…”

Section: Introductionmentioning

confidence: 99%

“…Hence, short bowel transit time (below 24 h) might support the fast-growing bacteria and can be a key factor to control the fermentation of dietary fibers in the colon. The study of Roager revealed associations of the colonic transit time and the overall gut microbial composition, diversity, and metabolism [4]. The longer colonic transit time was found to accompany with the higher microbial richness and a shift in colonic metabolism from carbohydrate fermentation to protein catabolism, while shorter transit time correlated with the metabolites possibly reﬂecting the increased renewal of the colonic mucosa.…”

Section: Introductionmentioning

confidence: 99%

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Selection of fast and slow growing bacteria from fecal microbiota using continuous culture with changing dilution rate

Adamberg

2018

Microbial Ecology in Health and Disease

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Background: Nutrient and energy metabolism in human colon depends on bacterial growth rate that is determined by the colonic transit rate.Objective: A novel approach, De-stat culture was used to distinguish the fast and slow growing sub-populations from fecal microbiota.Design: The enrichment and metabolism of bacteria from pooled fecal cultures of children was studied at dilution rates D = 0.2–0.0 1/h in mucin-supplemented media containing either arabinogalactan or apple pectin.Results: The study revealed clear differentiation of the fecal microbiota at higher (above 0.1 1/h) and lower (below 0.1 1/h) dilution rates, along with metabolic changes. Similarity of the fast and slow growing bacteria was observed in two different fecal pools and on both substrates, suggesting the dilution rate as the main triggering parameter for selection of bacteria. At high dilution rates, the species Collinsella aerofaciens, Dorea longicatena, Escherichia coli, Lachnoclostridium torques, and different Bacteroides (B. caccae, B. fragilis, B. ovatus, B. thetaiotaomicron, B. vulgatus) were dominant in both media variants. At low dilution rates, Akkermansia muciniphila, Eisenbergiella tayi, Negativicoccus succinivorans, and a group of Ruminococcaceae became dominant in both media and in both fecal pools. This change in bacterial population accompanied by the increased production of propionic and butyric acids as well as higher consumption of alanine and branched chain amino acids at low dilution rates.Conclusions: The study suggests that specific growth rate has important effect on the dynamics of colon microbiota. Manipulation of the proportions of fast and slow growing gut bacteria through modulation of the transit rate could be a target in human nutrition studies. The De-stat study would enable to predict changes in microbiota composition associated with the decrease or increase of the colonic transit rate.

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“…Blood levels of these toxins (e.g., p-cresol sulfate, indoxyl sulfate) increase when kidney function declines (16), and higher levels are directly associated with higher dietary protein and lower fiber intakes (41). Colonic transit time (i.e., the time it takes for digesta to move through the colon) also significantly impacts the gut microbiota and fermentation (40). Slow transit, commonly referred to as constipation, increases protein fermentation due to depletion of carbohydrate substrate (49).…”

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confidence: 99%

Pea Hull Fiber: A Dietary Fiber to Modulate Gastrointestinal Function and Gut Microbiota

Dahl

2017

Cereal Foods World

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Colonic transit time is related to bacterial metabolism and mucosal turnover in the gut

Cited by 358 publications

References 67 publications

Effect of water flow and chemical environment on microbiota growth and composition in the human colon

Effect of water flow and chemical environment on microbiota growth and composition in the human colon

Selection of fast and slow growing bacteria from fecal microbiota using continuous culture with changing dilution rate

Pea Hull Fiber: A Dietary Fiber to Modulate Gastrointestinal Function and Gut Microbiota

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