Composition and Metabolic Activities of Bacterial Biofilms Colonizing Food Residues in the Human Gut

Abstract

Bacteria growing in the human large intestine live in intimate association with the host and play an important role in host digestive processes, gut physiology, and metabolism. Fecal bacteria have been investigated extensively, but few studies have been done on biofilms that form on digestive wastes in the large bowel. The aims of this investigation were to investigate the composition and metabolic activities of bacterial communities that colonize the surfaces of food residues in fecal material, with respect to their role in the fermentation of complex carbohydrates. Fresh stools were obtained from 15 healthy donors, and food residues were separated by filtration. Adherent bacteria were removed by surfactant treatment for microbiological analysis and fermentation studies. Scanning electron microscopy and fluorescent in situ hybridization in conjunction with confocal laser scanning microscopy (CLSM) were used to visualize intact biofilms. Results showed that bacterial populations strongly adhering to particulate matter were phenotypically similar in composition to unattached communities, with bacteroides and bifidobacteria predominating. Biofilms comprised a mixture of living and dead bacteria, and CLSM showed that bifidobacteria in the biofilms occurred as isolated dispersed cells and in microcolonies near the interface with the substratum. Fermentation experiments with a variety of complex carbohydrates demonstrated that biofilm populations were more efficient in digesting polysaccharides, while nonadhering communities fermented oligosaccharides most rapidly. Acetate was the principal fermentation product formed by biofilm bacteria, whereas higher levels of butyrate were produced by nonadherent populations, showing that the two communities were metabolically distinct.The human colon is a highly specialized digestive organ that contains large numbers of bacteria that exist in stable complex communities. Bacteria are a major component of colonic material, comprising approximately 55% of solids in persons living on western-style diets (40), and the average daily fecal output is approximately 120 g (10). Many hundreds of different species and strains have been identified in intestinal contents (26) as well as on mucosal surfaces lining the bowel (30). The metabolic activities of the microbiota affect host physiology in a multiplicity of ways; through fermentation, for example, bacteria in the hindgut complete the digestive process and contribute to energy reclamation and host metabolism (11). The colonic epithelium has an obligate requirement for bacterial fermentation products (11), while the maintenance of colonization resistance to microbial pathogens (19), the activation or destruction of genotoxins and mutagens (33), and modulation of the immune system (39) are all dependent on the microbiota. Although host tissues and other endogenous substrates such as mucins, pancreatic enzymes, and other secretions are broken down and recycled by intestinal bacteria, the species composition and biochemical activities of th...

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