Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiae
ABSTRACT Increasing evidence suggests that in disease-suppressive soils, microbial volatile compounds (mVCs) released from bacteria may inhibit the growth of plant-pathogenic fungi. However, the antifungal activities and molecular responses of fungi to different mVCs remain largely undescribed. In t...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-10-01
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| Series: | mSphere |
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| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00324-23 |
| _version_ | 1797651054884552704 |
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| author | Tri-Phuong Nguyen De-Rui Meng Ching-Han Chang Pei-Yu Su Chieh-An Ou Ping-Fu Hou Huang-Mo Sung Chang-Hung Chou Masaru Ohme-Takagi Hao-Jen Huang |
| author_facet | Tri-Phuong Nguyen De-Rui Meng Ching-Han Chang Pei-Yu Su Chieh-An Ou Ping-Fu Hou Huang-Mo Sung Chang-Hung Chou Masaru Ohme-Takagi Hao-Jen Huang |
| author_sort | Tri-Phuong Nguyen |
| collection | DOAJ |
| description | ABSTRACT Increasing evidence suggests that in disease-suppressive soils, microbial volatile compounds (mVCs) released from bacteria may inhibit the growth of plant-pathogenic fungi. However, the antifungal activities and molecular responses of fungi to different mVCs remain largely undescribed. In this study, we first evaluated the responses of pathogenic fungi to treatment with mVCs from Paenarthrobacter ureafaciens. Then, we utilized the well-characterized fungal model organism Saccharomyces cerevisiae to study the potential mechanistic effects of the mVCs. Our data showed that exposure to P. ureafaciens mVCs leads to reduced growth of several pathogenic fungi, and in yeast cells, mVC exposure prompts the accumulation of reactive oxygen species. Further experiments with S. cerevisiae deletion mutants indicated that Slt2/Mpk1 and Hog1 MAPKs play major roles in the yeast response to P. ureafaciens mVCs. Transcriptomic analysis revealed that exposure to mVCs was associated with 1,030 differentially expressed genes (DEGs) in yeast. According to gene ontology and Kyoto Encyclopedia of Genes and Genomes analyses, many of these DEGs are involved in mitochondrial dysfunction, cell integrity, mitophagy, cellular metabolism, and iron uptake. Genes encoding antimicrobial proteins were also significantly altered in the yeast after exposure to mVCs. These findings suggest that oxidative damage and mitochondrial dysfunction are major contributors to the fungal toxicity of mVCs. Furthermore, our data showed that cell wall, antioxidant, and antimicrobial defenses are induced in yeast exposed to mVCs. Thus, our findings expand upon previous research by delineating the transcriptional responses of the fungal model. IMPORTANCE Since the use of bacteria-emitted volatile compounds in phytopathogen control is of considerable interest, it is important to understand the molecular mechanisms by which fungi may adapt to microbial volatile compounds (mVCs). Paenarthrobacter ureafaciens is an isolated bacterium from disease-suppressive soil that belongs to the Actinomycetota phylum. P. ureafaciens mVCs showed a potent antifungal effect on phytopathogens, which may contribute to disease suppression in soil. However, our knowledge about the antifungal mechanism of mVCs is limited. This study has proven that mVCs are toxic to fungi due to oxidative stress and mitochondrial dysfunction. To deal with mVC toxicity, antioxidants and physical defenses are required. Furthermore, iron uptake and CAP proteins are required for antimicrobial defense, which is necessary for fungi to deal with the thread from mVCs. This study provides essential foundational knowledge regarding the molecular responses of fungi to inhibitory mVCs. |
| first_indexed | 2024-03-11T16:09:28Z |
| format | Article |
| id | doaj.art-9e90ee35744f4399af8f7d9624e79b6c |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-03-11T16:09:28Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
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| series | mSphere |
| spelling | doaj.art-9e90ee35744f4399af8f7d9624e79b6c2023-10-24T16:32:15ZengAmerican Society for MicrobiologymSphere2379-50422023-10-018510.1128/msphere.00324-23Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiaeTri-Phuong Nguyen0De-Rui Meng1Ching-Han Chang2Pei-Yu Su3Chieh-An Ou4Ping-Fu Hou5Huang-Mo Sung6Chang-Hung Chou7Masaru Ohme-Takagi8Hao-Jen Huang9Department of Life Sciences, National Cheng Kung University , Tainan, TaiwanDepartment of Life Sciences, National Cheng Kung University , Tainan, TaiwanGraduate Program in Translational Agricultural Sciences, National Cheng Kung University and Academia Sinica , Tainan, TaiwanDepartment of Life Sciences, National Cheng Kung University , Tainan, TaiwanDepartment of Life Sciences, National Cheng Kung University , Tainan, TaiwanKaohsiung District Agricultural Research and Extension Station , Pingtung, TaiwanDepartment of Life Sciences, National Cheng Kung University , Tainan, TaiwanDepartment of Life Sciences, National Cheng Kung University , Tainan, TaiwanInstitute of Tropical Plant Sciences and Microbiology, National Cheng Kung University , Tainan, TaiwanDepartment of Life Sciences, National Cheng Kung University , Tainan, TaiwanABSTRACT Increasing evidence suggests that in disease-suppressive soils, microbial volatile compounds (mVCs) released from bacteria may inhibit the growth of plant-pathogenic fungi. However, the antifungal activities and molecular responses of fungi to different mVCs remain largely undescribed. In this study, we first evaluated the responses of pathogenic fungi to treatment with mVCs from Paenarthrobacter ureafaciens. Then, we utilized the well-characterized fungal model organism Saccharomyces cerevisiae to study the potential mechanistic effects of the mVCs. Our data showed that exposure to P. ureafaciens mVCs leads to reduced growth of several pathogenic fungi, and in yeast cells, mVC exposure prompts the accumulation of reactive oxygen species. Further experiments with S. cerevisiae deletion mutants indicated that Slt2/Mpk1 and Hog1 MAPKs play major roles in the yeast response to P. ureafaciens mVCs. Transcriptomic analysis revealed that exposure to mVCs was associated with 1,030 differentially expressed genes (DEGs) in yeast. According to gene ontology and Kyoto Encyclopedia of Genes and Genomes analyses, many of these DEGs are involved in mitochondrial dysfunction, cell integrity, mitophagy, cellular metabolism, and iron uptake. Genes encoding antimicrobial proteins were also significantly altered in the yeast after exposure to mVCs. These findings suggest that oxidative damage and mitochondrial dysfunction are major contributors to the fungal toxicity of mVCs. Furthermore, our data showed that cell wall, antioxidant, and antimicrobial defenses are induced in yeast exposed to mVCs. Thus, our findings expand upon previous research by delineating the transcriptional responses of the fungal model. IMPORTANCE Since the use of bacteria-emitted volatile compounds in phytopathogen control is of considerable interest, it is important to understand the molecular mechanisms by which fungi may adapt to microbial volatile compounds (mVCs). Paenarthrobacter ureafaciens is an isolated bacterium from disease-suppressive soil that belongs to the Actinomycetota phylum. P. ureafaciens mVCs showed a potent antifungal effect on phytopathogens, which may contribute to disease suppression in soil. However, our knowledge about the antifungal mechanism of mVCs is limited. This study has proven that mVCs are toxic to fungi due to oxidative stress and mitochondrial dysfunction. To deal with mVC toxicity, antioxidants and physical defenses are required. Furthermore, iron uptake and CAP proteins are required for antimicrobial defense, which is necessary for fungi to deal with the thread from mVCs. This study provides essential foundational knowledge regarding the molecular responses of fungi to inhibitory mVCs.https://journals.asm.org/doi/10.1128/msphere.00324-23Paenarthrobacter ureafaciensphytopathogensantifungal mechanismvolatile organic compoundsvolatile allelochemicalsallelopathy |
| spellingShingle | Tri-Phuong Nguyen De-Rui Meng Ching-Han Chang Pei-Yu Su Chieh-An Ou Ping-Fu Hou Huang-Mo Sung Chang-Hung Chou Masaru Ohme-Takagi Hao-Jen Huang Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiae mSphere Paenarthrobacter ureafaciens phytopathogens antifungal mechanism volatile organic compounds volatile allelochemicals allelopathy |
| title | Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiae |
| title_full | Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiae |
| title_fullStr | Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiae |
| title_full_unstemmed | Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiae |
| title_short | Antifungal mechanism of volatile compounds emitted by Actinomycetota Paenarthrobacter ureafaciens from a disease-suppressive soil on Saccharomyces cerevisiae |
| title_sort | antifungal mechanism of volatile compounds emitted by actinomycetota paenarthrobacter ureafaciens from a disease suppressive soil on saccharomyces cerevisiae |
| topic | Paenarthrobacter ureafaciens phytopathogens antifungal mechanism volatile organic compounds volatile allelochemicals allelopathy |
| url | https://journals.asm.org/doi/10.1128/msphere.00324-23 |
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