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

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  • Fanrui Hao

    (Yunnan University)

  • Huimin Liu

    (Yunnan University)

  • Bin Qi

    (Yunnan University)

Abstract

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 (UPRmt) by regulating the release of Neuropeptide-Like Protein (NLP-3). Interestingly, activating UPRmt 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.

Suggested Citation

  • Fanrui Hao & Huimin Liu & Bin Qi, 2024. "Bacterial peptidoglycan acts as a digestive signal mediating host adaptation to diverse food resources in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47530-y
    DOI: 10.1038/s41467-024-47530-y
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    1. Verónica Donato & Facundo Rodríguez Ayala & Sebastián Cogliati & Carlos Bauman & Juan Gabriel Costa & Cecilia Leñini & Roberto Grau, 2017. "Bacillus subtilis biofilm extends Caenorhabditis elegans longevity through downregulation of the insulin-like signalling pathway," Nature Communications, Nature, vol. 8(1), pages 1-15, April.
    2. Ravi S. Kamath & Andrew G. Fraser & Yan Dong & Gino Poulin & Richard Durbin & Monica Gotta & Alexander Kanapin & Nathalie Le Bot & Sergio Moreno & Marc Sohrmann & David P. Welchman & Peder Zipperlen &, 2003. "Systematic functional analysis of the Caenorhabditis elegans genome using RNAi," Nature, Nature, vol. 421(6920), pages 231-237, January.
    3. Ping Zhou & Yang She & Na Dong & Peng Li & Huabin He & Alessio Borio & Qingcui Wu & Shan Lu & Xiaojun Ding & Yong Cao & Yue Xu & Wenqing Gao & Mengqiu Dong & Jingjin Ding & Da-Cheng Wang & Alla Zamyat, 2018. "Alpha-kinase 1 is a cytosolic innate immune receptor for bacterial ADP-heptose," Nature, Nature, vol. 561(7721), pages 122-126, September.
    4. Nico Eisenhauer & Carlos A. Guerra, 2019. "Global maps of soil-dwelling nematode worms," Nature, Nature, vol. 572(7768), pages 187-188, August.
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