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Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria
Nematodes feed mainly on bacteria and sense volatile signals through their chemosensory system to distinguish food from pathogens. Although nematodes recognizing bacteria by volatile metabolites are ubiquitous, little is known of the associated molecular mechanism. Here, we show that the antinematod...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927473/ https://www.ncbi.nlm.nih.gov/pubmed/36511721 http://dx.doi.org/10.1128/spectrum.02319-22 |
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author | Cheng, Wanli Xue, Hua Yang, Xue Huang, Dian Cai, Minmin Huang, Feng Zheng, Longyu Peng, Donghai Thomashow, Linda S. Weller, David M. Yu, Ziniu Zhang, Jibin |
author_facet | Cheng, Wanli Xue, Hua Yang, Xue Huang, Dian Cai, Minmin Huang, Feng Zheng, Longyu Peng, Donghai Thomashow, Linda S. Weller, David M. Yu, Ziniu Zhang, Jibin |
author_sort | Cheng, Wanli |
collection | PubMed |
description | Nematodes feed mainly on bacteria and sense volatile signals through their chemosensory system to distinguish food from pathogens. Although nematodes recognizing bacteria by volatile metabolites are ubiquitous, little is known of the associated molecular mechanism. Here, we show that the antinematode bacterium Paenibacillus polymyxa KM2501-1 exhibits an attractive effect on Caenorhabditis elegans via volatile metabolites, of which furfural acetone (FAc) acts as a broad-spectrum nematode attractant. We show that the attractive response toward FAc requires both the G-protein-coupled receptors STR-2 in AWC neurons and SRA-13 in AWA and AWC neurons. In the downstream olfactory signaling cascades, both the transient receptor potential vanilloid channel and the cyclic nucleotide-gated channel are necessary for FAc sensation. These results indicate that multiple receptors and subsequent signaling cascades contribute to the attractive response of C. elegans to FAc, and FAc is the first reported ligand of SRA-13. Our current work discovers that P. polymyxa KM2501-1 exhibits an attractive effect on nematodes by secreting volatile metabolites, especially FAc and 2-heptanone, broadening our understanding of the interactions between bacterial pathogens and nematodes. IMPORTANCE Nematodes feed on nontoxic bacteria as a food resource and avoid toxic bacteria; they distinguish them through their volatile metabolites. However, the mechanism of how nematodes recognize bacteria by volatile metabolites is not fully understood. Here, the antinematode bacterium Paenibacillus polymyxa KM2501-1 is found to exhibit an attractive effect on Caenorhabditis elegans via volatile metabolites, including FAc. We further reveal that the attractive response of C. elegans toward FAc requires multiple G-protein-coupled receptors and downstream olfactory signaling cascades in AWA and AWC neurons. This study highlights the important role of volatile metabolites in the interaction between nematodes and bacteria and confirms that multiple G-protein-coupled receptors on different olfactory neurons of C. elegans can jointly sense bacterial volatile signals. |
format | Online Article Text |
id | pubmed-9927473 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-99274732023-02-15 Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria Cheng, Wanli Xue, Hua Yang, Xue Huang, Dian Cai, Minmin Huang, Feng Zheng, Longyu Peng, Donghai Thomashow, Linda S. Weller, David M. Yu, Ziniu Zhang, Jibin Microbiol Spectr Research Article Nematodes feed mainly on bacteria and sense volatile signals through their chemosensory system to distinguish food from pathogens. Although nematodes recognizing bacteria by volatile metabolites are ubiquitous, little is known of the associated molecular mechanism. Here, we show that the antinematode bacterium Paenibacillus polymyxa KM2501-1 exhibits an attractive effect on Caenorhabditis elegans via volatile metabolites, of which furfural acetone (FAc) acts as a broad-spectrum nematode attractant. We show that the attractive response toward FAc requires both the G-protein-coupled receptors STR-2 in AWC neurons and SRA-13 in AWA and AWC neurons. In the downstream olfactory signaling cascades, both the transient receptor potential vanilloid channel and the cyclic nucleotide-gated channel are necessary for FAc sensation. These results indicate that multiple receptors and subsequent signaling cascades contribute to the attractive response of C. elegans to FAc, and FAc is the first reported ligand of SRA-13. Our current work discovers that P. polymyxa KM2501-1 exhibits an attractive effect on nematodes by secreting volatile metabolites, especially FAc and 2-heptanone, broadening our understanding of the interactions between bacterial pathogens and nematodes. IMPORTANCE Nematodes feed on nontoxic bacteria as a food resource and avoid toxic bacteria; they distinguish them through their volatile metabolites. However, the mechanism of how nematodes recognize bacteria by volatile metabolites is not fully understood. Here, the antinematode bacterium Paenibacillus polymyxa KM2501-1 is found to exhibit an attractive effect on Caenorhabditis elegans via volatile metabolites, including FAc. We further reveal that the attractive response of C. elegans toward FAc requires multiple G-protein-coupled receptors and downstream olfactory signaling cascades in AWA and AWC neurons. This study highlights the important role of volatile metabolites in the interaction between nematodes and bacteria and confirms that multiple G-protein-coupled receptors on different olfactory neurons of C. elegans can jointly sense bacterial volatile signals. American Society for Microbiology 2022-12-13 /pmc/articles/PMC9927473/ /pubmed/36511721 http://dx.doi.org/10.1128/spectrum.02319-22 Text en Copyright © 2022 Cheng et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Cheng, Wanli Xue, Hua Yang, Xue Huang, Dian Cai, Minmin Huang, Feng Zheng, Longyu Peng, Donghai Thomashow, Linda S. Weller, David M. Yu, Ziniu Zhang, Jibin Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria |
title | Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria |
title_full | Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria |
title_fullStr | Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria |
title_full_unstemmed | Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria |
title_short | Multiple Receptors Contribute to the Attractive Response of Caenorhabditis elegans to Pathogenic Bacteria |
title_sort | multiple receptors contribute to the attractive response of caenorhabditis elegans to pathogenic bacteria |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9927473/ https://www.ncbi.nlm.nih.gov/pubmed/36511721 http://dx.doi.org/10.1128/spectrum.02319-22 |
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