Abstract
The gut microbiota represent a highly complex ecosystem comprised of approximately 1000 species that forms a mutualistic relationship with the human host. A critical attribute of the microbiota is high species diversity, which provides system robustness through overlapping and redundant metabolic capabilities. The gradual loss of bacterial diversity has been associated with a broad array of gut pathologies and diseases including malnutrition, obesity, diabetes and inflammatory bowel disease. We formulated an in silico community model of the gut microbiota by combining genome-scale metabolic reconstructions of 28 representative species to explore the relationship between species diversity and community growth. While the individual species offered a broad range of metabolic capabilities, communities optimized for maximal growth on simulated Western and high-fiber diets had low diversities and imbalances in short-chain fatty acid (SCFA) synthesis characterized by acetate overproduction. Community flux variability analysis performed with the 28-species model and a reduced 20-species model suggested that enhanced species diversity and more balanced SCFA production were achievable at suboptimal growth rates. We developed a simple method for constraining species abundances to sample the growth-diversity tradeoff and used the 20-species model to show that tradeoff curves for Western and high-fiber diets resembled Pareto-optimal surfaces. Compared to maximal growth solutions, suboptimal growth solutions were characterized by higher species diversity, more balanced SCFA synthesis and lower exchange rates of crossfed metabolites between more species. We hypothesized that modulation of crossfeeding relationships through host-microbiota interactions could be an important means for maintaining species diversity and suggest that community metabolic modeling approaches that allow multiobjective optimization of growth and diversity are needed for more realistic simulation of complex communities.
Highlights
The gut microbiota comprise a highly complex ecosystem that has been characterized as an additional organ within the human host [1, 2]
The gut microbiota serve a critical role in maintaining a healthy state in the human host
Suboptimal community growth promotes species diversity in the gut microbiota from these grants were used to cover the costs to publish in open access
Summary
The gut microbiota comprise a highly complex ecosystem that has been characterized as an additional organ within the human host [1, 2]. The microbiota form a mutualistic relationship with the host, with saccharolytic species enzymatically degrading complex carbohydrates into fermentable sugars and fermentative species converting sugars and other available nutrients into a variety of absorbable metabolites [3, 4]. A important function of the microbiota is to ferment dietary fiber into the short-chain fatty acids (SCFAs) acetate, butyrate and propionate [5, 6]. While significant variations are possible depending on diet, the molar ratio of these three SCFAs is approximately 60:20:20 [7]. The gut microbiota consist of approximately 1,000 species [8] and 7,000 unique strains [2] SCFAs are consumed by host colonocytes as a primary energy source, with butyrate being the preferred SCFA but acetate probably supplying more energy to its higher concentration in vivo.
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