Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths
Abstract Interactions among insects, plants, and microorganisms are fundamental to ecosystem dynamics, with floral nectar and pollen serving as key resources for various organisms. Yeasts, such as Metschnikowia reukaufii, commonly found in nectar, influence nectarial attraction through volatile comp...
Saved in:
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2025-02-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-56354-3 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850196851694764032 |
|---|---|
| author | Baiwei Ma Hetan Chang Mengbo Guo Dong Ai Jiayu Wang Run Chen Xiaolan Liu Bingzhong Ren Bill S. Hansson Guirong Wang |
| author_facet | Baiwei Ma Hetan Chang Mengbo Guo Dong Ai Jiayu Wang Run Chen Xiaolan Liu Bingzhong Ren Bill S. Hansson Guirong Wang |
| author_sort | Baiwei Ma |
| collection | DOAJ |
| description | Abstract Interactions among insects, plants, and microorganisms are fundamental to ecosystem dynamics, with floral nectar and pollen serving as key resources for various organisms. Yeasts, such as Metschnikowia reukaufii, commonly found in nectar, influence nectarial attraction through volatile compounds (VOCs), yet the underlying biological mechanisms remain elusive. Here, we show that isoamyl alcohol, a prominent yeast VOC, attracts oriental armyworm moths (Mythimna separata) to pollen-rich, yeast-fermented nectar. In a series of electrophysiological and behavioral assays, we show that isoamyl alcohol activates a single class of highly specific olfactory sensory neurons expressing the olfactory receptor MsepOR8. In the moth antennal lobe, these neurons target the AM2 glomerulus, which responds to isoamyl alcohol. Genetic disruption of MsepOR8 leads to complete abolition of both physiological and behavioral responses to isoamyl alcohol, resulting in an impaired ability to locate nectar sources. Moreover, we show that isoamyl alcohol-induced foraging behavior fosters a mutualistic relationship between yeast and moths to some extent, enhancing yeast dispersal and increasing moth reproductive success. Our results unveil a highly specific mechanism by which a yeast-derived VOC facilitates insect-yeast mutualism, providing insights into insect-microbe interactions within pollination ecosystems. |
| format | Article |
| id | doaj-art-bd3bd1e032be4f9e8f01f756837275f2 |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-bd3bd1e032be4f9e8f01f756837275f22025-08-20T02:13:20ZengNature PortfolioNature Communications2041-17232025-02-0116111410.1038/s41467-025-56354-3Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm mothsBaiwei Ma0Hetan Chang1Mengbo Guo2Dong Ai3Jiayu Wang4Run Chen5Xiaolan Liu6Bingzhong Ren7Bill S. Hansson8Guirong Wang9Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Synthetic Biology Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesShenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Synthetic Biology Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesZhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects; Department of Plant Protection, Advanced College of Agricultural Sciences, Zhejiang A & F UniversityState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesShenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Synthetic Biology Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesJilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, School of Life Sciences, Northeast Normal UniversityDepartment of Evolutionary Neuroethology, Max Planck Institute for Chemical EcologyShenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Synthetic Biology Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural SciencesAbstract Interactions among insects, plants, and microorganisms are fundamental to ecosystem dynamics, with floral nectar and pollen serving as key resources for various organisms. Yeasts, such as Metschnikowia reukaufii, commonly found in nectar, influence nectarial attraction through volatile compounds (VOCs), yet the underlying biological mechanisms remain elusive. Here, we show that isoamyl alcohol, a prominent yeast VOC, attracts oriental armyworm moths (Mythimna separata) to pollen-rich, yeast-fermented nectar. In a series of electrophysiological and behavioral assays, we show that isoamyl alcohol activates a single class of highly specific olfactory sensory neurons expressing the olfactory receptor MsepOR8. In the moth antennal lobe, these neurons target the AM2 glomerulus, which responds to isoamyl alcohol. Genetic disruption of MsepOR8 leads to complete abolition of both physiological and behavioral responses to isoamyl alcohol, resulting in an impaired ability to locate nectar sources. Moreover, we show that isoamyl alcohol-induced foraging behavior fosters a mutualistic relationship between yeast and moths to some extent, enhancing yeast dispersal and increasing moth reproductive success. Our results unveil a highly specific mechanism by which a yeast-derived VOC facilitates insect-yeast mutualism, providing insights into insect-microbe interactions within pollination ecosystems.https://doi.org/10.1038/s41467-025-56354-3 |
| spellingShingle | Baiwei Ma Hetan Chang Mengbo Guo Dong Ai Jiayu Wang Run Chen Xiaolan Liu Bingzhong Ren Bill S. Hansson Guirong Wang Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths Nature Communications |
| title | Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths |
| title_full | Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths |
| title_fullStr | Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths |
| title_full_unstemmed | Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths |
| title_short | Yeast-derived volatiles orchestrate an insect-yeast mutualism with oriental armyworm moths |
| title_sort | yeast derived volatiles orchestrate an insect yeast mutualism with oriental armyworm moths |
| url | https://doi.org/10.1038/s41467-025-56354-3 |
| work_keys_str_mv | AT baiweima yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT hetanchang yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT mengboguo yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT dongai yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT jiayuwang yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT runchen yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT xiaolanliu yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT bingzhongren yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT billshansson yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths AT guirongwang yeastderivedvolatilesorchestrateaninsectyeastmutualismwithorientalarmywormmoths |