Nutrition of Escherichia coli within the intestinal microbiome

Abstract

In this chapter, we update our 2004 review of "The Life of Commensal Escherichia coli in the Mammalian Intestine" (https://doi.org/10.1128/ecosalplus.8.3.1.2), with a change of title that reflects the current focus on "Nutrition of E. coli within the Intestinal Microbiome." The earlier part of the previous two decades saw incremental improvements in understanding the carbon and energy sources that E. coli and Salmonella use to support intestinal colonization. Along with these investigations of electron donors came a better understanding of the electron acceptors that support the respiration of these facultative anaerobes in the gastrointestinal tract. Hundreds of recent papers add to what was known about the nutrition of commensal and pathogenic enteric bacteria. The fact that each biotype or pathotype grows on a different subset of the available nutrients suggested a mechanism for succession of commensal colonizers and invasion by enteric pathogens. Competition for nutrients in the intestine has also come to be recognized as one basis for colonization resistance, in which colonized strain(s) prevent colonization by a challenger. In the past decade, detailed investigations of fiber- and mucin-degrading anaerobes added greatly to our understanding of how complex polysaccharides support the hundreds of intestinal microbiome species. It is now clear that facultative anaerobes, which usually cannot degrade complex polysaccharides, live in symbiosis with the anaerobic degraders. This concept led to the "restaurant hypothesis," which emphasizes that facultative bacteria, such as E. coli, colonize the intestine as members of mixed biofilms and obtain the sugars they need for growth locally through cross-feeding from polysaccharide-degrading anaerobes. Each restaurant represents an intestinal niche. Competition for those niches determines whether or not invaders are able to overcome colonization resistance and become established. Topics centered on the nutritional basis of intestinal colonization and gastrointestinal health are explored here in detail.

Keywords: E. coli; colonization; colonization resistance; intestine; microbiome; nutrition.

Fig 1

Illustration of how E. coli (A) obtains nutrients in the mucosal layer of the large intestine. Anaerobes (B) produce glycosyl hydrolases (C) which degrade complex polysaccharides in dietary fibers and mucin (D) to release oligosaccharides (E), disaccharides (F), and monosaccharides (G). Oligosaccharides are preferred by anaerobes, while monosaccharides and disaccharides are preferred by E. coli.

Fig 2

Four strategies used by an invading bacterium (blue) to compete for nutrients (represented by colored triangles and squares) with resident microbiota; anaerobes are shown in green and black, and facultative anaerobes are shown in red and pink. (A) Invader utilizes nutrients (white squares) not used by other members of the microbiota, and hence, does not have to compete for the nutrients. (B) Invader utilizes at least one nutrient (green triangles) faster than other members of the microbiota [in this case, another facultative anaerobe (red)]; this provides an advantage over the competing microbiota. (C) Invader occupies a distinct niche in the intestine where it uses a nutrient (magenta squares) that is locally available. Although the invader may fail to compete with the microbiota in major niches, it will thrive on a locally available nutrient. (D) Invader acquires some nutrients directly from the host cell using a nanotube, so it does not have to compete with other bacteria for nutrients (created with BioRender.com).