Lactate- and acetate-based cross-feeding interactions between selected strains of lactobacilli, bifidobacteria and colon bacteria in the presence of inulin-type fructans

Moens, Frédéric; Verce, Marko; Vuyst, Luc De

doi:10.1016/j.ijfoodmicro.2016.10.019

Cited by 128 publications

(105 citation statements)

References 70 publications

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“…Many of these metabolites are known to be involved in bacterial cross-feeding in the colon or cecum (for interconversion between acetate and lactate, see Ref. [40]; and for interconversion between acetate and butyrate in the murine cecum, see Ref. [41]).…”

Section: Resultsmentioning

confidence: 99%

Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism

Hoek

Merks

2017

BMC Syst Biol

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BackgroundThe human gut contains approximately 1014 bacteria, belonging to hundreds of different species. Together, these microbial species form a complex food web that can break down nutrient sources that our own digestive enzymes cannot handle, including complex polysaccharides, producing short chain fatty acids and additional metabolites, e.g., vitamin K. Microbial diversity is important for colonic health: Changes in the composition of the microbiota have been associated with inflammatory bowel disease, diabetes, obesity and Crohn’s disease, and make the microbiota more vulnerable to infestation by harmful species, e.g., Clostridium difficile. To get a grip on the controlling factors of microbial diversity in the gut, we here propose a multi-scale, spatiotemporal dynamic flux-balance analysis model to study the emergence of metabolic diversity in a spatial gut-like, tubular environment. The model features genome-scale metabolic models (GEM) of microbial populations, resource sharing via extracellular metabolites, and spatial population dynamics and evolution.ResultsIn this model, cross-feeding interactions emerge readily, despite the species’ ability to metabolize sugars autonomously. Interestingly, the community requires cross-feeding for producing a realistic set of short-chain fatty acids from an input of glucose, If we let the composition of the microbial subpopulations change during invasion of adjacent space, a complex and stratified microbiota evolves, with subspecies specializing on cross-feeding interactions via a mechanism of compensated trait loss. The microbial diversity and stratification collapse if the flux through the gut is enhanced to mimic diarrhea.ConclusionsIn conclusion, this in silico model is a helpful tool in systems biology to predict and explain the controlling factors of microbial diversity in the gut. It can be extended to include, e.g., complex nutrient sources, and host-microbiota interactions via the intestinal wall.Electronic supplementary materialThe online version of this article (doi:10.1186/s12918-017-0430-4) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 99%

Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism

Hoek

Merks

2017

BMC Syst Biol

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“…While we and others have shown that epithelial cells can make and release IL-10 in response to a number of stimuli (46–48), it is possible that butyrate also induces IL-10 mRNA degradation. IL10 mRNA, for example, is known to be degraded through processing at the 3′UTR by live probiotic bacteria including Lactobacillus paracasei (49), a known butyrate producer (50). It is also possible that the low concentrations of IL-10 protein measured in tissue culture bulk flow are sufficient at the cell surface to activate butyrate-induced IL-10RA.…”

Section: Discussionmentioning

confidence: 99%

Microbial-Derived Butyrate Promotes Epithelial Barrier Function through IL-10 Receptor–Dependent Repression of Claudin-2

Zheng

Kelly

Battista

et al. 2017

The Journal of Immunology

378

260

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Commensal interactions between the enteric microbiota and distal intestine play important roles in regulating human health. Short-chain fatty acids (SCFAs), such as butyrate, produced through anaerobic microbial metabolism represent a major energy source for the host colonic epithelium and enhance epithelial barrier function through unclear mechanisms. Separate studies revealed that the epithelial anti-inflammatory interleukin-10 receptor α-subunit (IL-10RA) is also important for barrier formation. Based on these findings, we examined if SCFAs promote epithelial barrier through IL-10RA-dependent mechanisms. Using human intestinal epithelial cells (IECs), we discovered that SCFAs, particularly butyrate, enhanced IEC barrier formation, induced IL10RA mRNA, IL-10RA protein, and transactivation through activated Stat3 and HDAC inhibition. Loss and gain of IL10RA expression directly correlates with IEC barrier formation and butyrate represses permeability-promoting claudin-2 (Cldn2) tight-junction protein expression through an IL-10RA-dependent mechanism. Our findings provide a novel mechanism by which microbial-derived butyrate promotes barrier through IL-10RA-dependent repression of Cldn2.

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“…While formate is rarely highlighted as a key intermediate in gut cross-feeding interactions, it has been reported to be an end-product of primary polysaccharide degradation by both Bifidobacterium and Lactobacillus spp. (Falony, Lazidou et al, 2009b, Moens et al, 2017. Hence, our results invite a re-evaluation of the ecological niche of BH in relation with microbial formate production potential.…”

Section: Discussionmentioning

confidence: 61%

“…In vitro studies of human gut microorganisms have a long tradition and have been carried out in several manners. Classical mono-and coculture studies in batch and chemostat fermentors have explored nutrient preferences and interaction mechanisms (Falony, Calmeyn et al, 2009a, Falony, Vlachou et al, 2006, Moens, Verce et al, 2017, Moens, Weckx et al, 2016, Rivière, Selak et al, 2016. Artificial gut systems, such as the TNO In Vitro Model of the Colon (TIM-2) (Venema, 2015) and the Simulation of the Human Intestinal Microbial Ecosystem (SHIME) (T. Van de Wiele, P. Van den Abbeele et al, 2015), seek to reproduce as closely as possible the conditions of the human gastrointestinal tract in a well-controlled manner.…”

Section: Introductionmentioning

confidence: 99%

Integrated culturing, modeling and transcriptomics uncovers complex interactions and emergent behavior in a synthetic gut community

D’hoe

Vet

Faust

et al. 2018

Preprint

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Whereas the composition of the human gut microbiome is relatively well resolved, predictive understanding of its response to perturbations such as diet shifts is still lacking. Here, we followed a bottom-up strategy to explore human gut community dynamics. We established a synthetic community composed of three representative human gut isolates in well-controlled conditions in vitro. We then explored species interactions by performing all mono-and pair-wise fermentation experiments and quantified with a mechanistic community model how well tri-culture dynamics was predicted from mono-culture data. With the model as a reference, we demonstrated that species grown in co-culture behaved differently than in mono-culture and confirmed their altered behavior at the transcriptional level. In addition, we showed with replicate tri-cultures and in simulations that dominance in tri-culture sensitively depends on initial conditions. Our work has important implications for gut microbial community modeling as well as ecological interaction detection from batch cultures.

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Lactate- and acetate-based cross-feeding interactions between selected strains of lactobacilli, bifidobacteria and colon bacteria in the presence of inulin-type fructans

Cited by 128 publications

References 70 publications

Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism

Emergence of microbial diversity due to cross-feeding interactions in a spatial model of gut microbial metabolism

Microbial-Derived Butyrate Promotes Epithelial Barrier Function through IL-10 Receptor–Dependent Repression of Claudin-2

Integrated culturing, modeling and transcriptomics uncovers complex interactions and emergent behavior in a synthetic gut community

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