Enhancing nutritional niche and host defenses by modifying the gut microbiome

• Published in: Molecular systems biology 2022-11, Vol.18 (11), p.e9933-n/a
• Main Authors: Sun, Qing, Vega, Nic M, Cervantes, Bernardo, Mancuso, Christopher P, Mao, Ning, Taylor, Megan N, Collins, James J, Khalil, Ahmad S, Gore, Jeff, Lu, Timothy K
• Format: Article
• Language: English
• Subjects: Animals; Bacteria; bacteria community; Caenorhabditis elegans - microbiology; Carbohydrates; Carbon; Carbon sources; Cellulase; Cellulolytic bacteria; Cellulose; Digestive system; E coli; EMBO23; EMBO41; Enzymes; Experiments; Food processing; Gastrointestinal Microbiome; Glucose; gut microbiome; Intestinal microflora; Metabolism; Microbiomes; Microbiota; Nematodes; Nutrient sources; Nutrients; Nutrition; Nutritional status; pathogen; Pathogens; Substrates; Worms
• ISSN: 1744-4292; 1744-4292
• DOI: 10.15252/msb.20209933

The gut microbiome is essential for processing complex food compounds and synthesizing nutrients that the host cannot digest or produce, respectively. New model systems are needed to study how the metabolic capacity provided by the gut microbiome impacts the nutritional status of the host, and to explore possibilities for altering host metabolic capacity via the microbiome. Here, we colonized the nematode Caenorhabditis elegans gut with cellulolytic bacteria that enabled C. elegans to utilize cellulose, an otherwise indigestible substrate, as a carbon source. Cellulolytic bacteria as a community component in the worm gut can also support additional bacterial species with specialized roles, which we demonstrate by using Lactobacillus plantarum to protect C. elegans against Salmonella enterica infection. This work shows that engineered microbiome communities can be used to endow host organisms with novel functions, such as the ability to utilize alternate nutrient sources or to better fight pathogenic bacteria. Synopsis A microbe‐host interaction model is developed by colonizing C. elegans with functional bacteria that allow digesting long‐chain cellulose. Direct benefits include increased host larval yield and protection of other gut species against pathogens. Heterologous bacteria (e.g. Pseudomonas cellulosa ) in the gut can help C. elegans to digest cellulose, an otherwise indigestible carbon substrate. Cellulolytic bacteria can also support other bacterial species with specialized roles: Lactobacillus protected the worms against Salmonella infection, and interspecies synergy between P. cellulosa and L. plantarum conferred benefit to the host. Engineered microbiome communities may provide host organisms with novel functions, including the ability to use complex nutrient sources and to fight pathogens. C. elegans colonized with bacteria provides a model system for studying microbiome‐host interactions. Graphical Abstract A microbe‐host interaction model is developed by colonizing C. elegans with functional bacteria that allow digesting long‐chain cellulose. Direct benefits include increased host larval yield and protection of other gut species against pathogens.