Bacterial peptidoglycan acts as a digestive signal mediating host adaptation to diverse food resources in C. elegans

• Published in: Nature communications 2024-04, Vol.15 (1), p.3286-15, Article 3286
• Main Authors: Hao, Fanrui, Liu, Huimin, Qi, Bin
• Format: Article
• Language: English
• Subjects: 13/89; 13/95; 14/63; 631/443/319/1488; 64/11; 692/4020/2741/2135; 82/80; Adaptation; Animal growth; Animals; Bacteria; Caenorhabditis elegans - metabolism; Caenorhabditis elegans Proteins - metabolism; Colonization; Colonization factor; Defects; Digestion; Digestive system; Food; Food availability; Food consumption; Food resources; Host Adaptation; Humanities and Social Sciences; MAP kinase; multidisciplinary; Natural environment; Peptidoglycan - metabolism; Peptidoglycans; Protein folding; Proteins; Science; Science (multidisciplinary)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-47530-y

Food availability and usage is a major adaptive force for the successful survival of animals in nature, yet little is known about the specific signals that activate the host digestive system to allow for the consumption of varied foods. Here, by using a food digestion system in C. elegans , we discover that bacterial peptidoglycan (PGN) is a unique food signal that activates animals to digest inedible food. We identified that a glycosylated protein, Bacterial Colonization Factor-1 (BCF-1), in the gut interacts with bacterial PGN, leading to the inhibition of the mitochondrial unfolded protein response (UPR mt ) by regulating the release of Neuropeptide-Like Protein (NLP-3). Interestingly, activating UPR mt was found to hinder food digestion, which depends on the innate immune p38 MAPK/PMK-1 pathway. Conversely, inhibiting PMK-1 was able to alleviate digestion defects in bcf-1 mutants. Furthermore, we demonstrate that animals with digestion defects experience reduced natural adaptation capabilities. This study reveals that PGN-BCF-1 interaction acts as “good-food signal” to promote food digestion and animal growth, which facilitates adaptation of the host animals by increasing ability to consume a wide range of foods in their natural environment. Here, by using a food digestion model in C. elegans , the authors identify a mechanism by which bacterial peptidoglycan (PGN) interacts with Bacterial Colonization Factor-1 (BCF-1) triggering C. elegans to expand its ability to consume a wide range of foods in their natural environment.