Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulum
ABSTRACT Accurately recognizing pathogens by the host is vital for initiating appropriate immune response against infecting microorganisms. Caenorhabditis elegans has no known receptor to recognize pathogen-associated molecular pattern. However, recent studies showed that nematodes have a strong spe...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01270-23 |
| _version_ | 1797658220179750912 |
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| author | Xue-Mei Zhuang Zhi-Yi Guo Meng Zhang Yong-Hong Chen Feng-Na Qi Ren-Qiao Wang Ling Zhang Pei-Ji Zhao Chao-Jun Lu Cheng-Gang Zou Yi-Cheng Ma Jianping Xu Ke-Qin Zhang Yan-Ru Cao Lian-Ming Liang |
| author_facet | Xue-Mei Zhuang Zhi-Yi Guo Meng Zhang Yong-Hong Chen Feng-Na Qi Ren-Qiao Wang Ling Zhang Pei-Ji Zhao Chao-Jun Lu Cheng-Gang Zou Yi-Cheng Ma Jianping Xu Ke-Qin Zhang Yan-Ru Cao Lian-Ming Liang |
| author_sort | Xue-Mei Zhuang |
| collection | DOAJ |
| description | ABSTRACT Accurately recognizing pathogens by the host is vital for initiating appropriate immune response against infecting microorganisms. Caenorhabditis elegans has no known receptor to recognize pathogen-associated molecular pattern. However, recent studies showed that nematodes have a strong specificity for transcriptomes infected by different pathogens, indicating that they can identify different pathogenic microorganisms. However, the mechanism(s) for such specificity remains largely unknown. In this study, we showed that the nematophagous fungus Purpureocillium lavendulum can infect the intestinal tract of the nematode C. elegans and the infection led to the accumulation of reactive oxygen species (ROS) in the infected intestinal tract, which suppressed fungal growth. Co-transcriptional analysis revealed that fungal genes related to anaerobic respiration and ethanol production were up-regulated during infection. Meanwhile, the ethanol dehydrogenase Sodh-1 in C. elegans was also up-regulated. Together, these results suggested that the infecting fungi encounter hypoxia stress in the nematode gut and that ethanol may play a role in the host–pathogen interaction. Ethanol production in vitro during fungal cultivation in hypoxia conditions was confirmed by gas chromatography-mass spectrometry. Direct treatment of C. elegans with ethanol elevated the sodh-1 expression and ROS accumulation while repressing a series of immunity genes that were also repressed during fungal infection. Mutation of sodh-1 in C. elegans blocked ROS accumulation and increased the nematode’s susceptibility to fungal infection. Our study revealed a new recognition and antifungal mechanism in C. elegans. The novel mechanism of ethanol-mediated interaction between the fungus and nematode provides new insights into fungal pathogenesis and for developing alternative biocontrol of pathogenic nematodes by nematophagous fungi. IMPORTANCE Nematodes are among the most abundant animals on our planet. Many of them are parasites in animals and plants and cause human and animal health problems as well as agricultural losses. Studying the interaction of nematodes and their microbial pathogens is of great importance for the biocontrol of animal and plant parasitic nematodes. In this study, we found that the model nematode Caenorhabditis elegans can recognize its fungal pathogen, the nematophagous fungus Purpureocillium lavendulum, through fungal-produced ethanol. Then the nematode elevated the reactive oxygen species production in the gut to inhibit fungal growth in an ethanol dehydrogenase-dependent manner. With this mechanism, novel biocontrol strategies may be developed targeting the ethanol receptor or metabolic pathway of nematodes. Meanwhile, as a volatile organic compound, ethanol should be taken seriously as a vector molecule in the microbial–host interaction in nature. |
| first_indexed | 2024-03-11T17:56:05Z |
| format | Article |
| id | doaj.art-6278550aaacc4a4fbf9bfd8933d1de43 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-11T17:56:05Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
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| series | Microbiology Spectrum |
| spelling | doaj.art-6278550aaacc4a4fbf9bfd8933d1de432023-10-17T13:04:35ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-10-0111510.1128/spectrum.01270-23Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulumXue-Mei Zhuang0Zhi-Yi Guo1Meng Zhang2Yong-Hong Chen3Feng-Na Qi4Ren-Qiao Wang5Ling Zhang6Pei-Ji Zhao7Chao-Jun Lu8Cheng-Gang Zou9Yi-Cheng Ma10Jianping Xu11Ke-Qin Zhang12Yan-Ru Cao13Lian-Ming Liang14State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaCollege of Agriculture and Life Sciences, Kunming University , Kunming, ChinaState Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan and The Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University , Kunming, ChinaABSTRACT Accurately recognizing pathogens by the host is vital for initiating appropriate immune response against infecting microorganisms. Caenorhabditis elegans has no known receptor to recognize pathogen-associated molecular pattern. However, recent studies showed that nematodes have a strong specificity for transcriptomes infected by different pathogens, indicating that they can identify different pathogenic microorganisms. However, the mechanism(s) for such specificity remains largely unknown. In this study, we showed that the nematophagous fungus Purpureocillium lavendulum can infect the intestinal tract of the nematode C. elegans and the infection led to the accumulation of reactive oxygen species (ROS) in the infected intestinal tract, which suppressed fungal growth. Co-transcriptional analysis revealed that fungal genes related to anaerobic respiration and ethanol production were up-regulated during infection. Meanwhile, the ethanol dehydrogenase Sodh-1 in C. elegans was also up-regulated. Together, these results suggested that the infecting fungi encounter hypoxia stress in the nematode gut and that ethanol may play a role in the host–pathogen interaction. Ethanol production in vitro during fungal cultivation in hypoxia conditions was confirmed by gas chromatography-mass spectrometry. Direct treatment of C. elegans with ethanol elevated the sodh-1 expression and ROS accumulation while repressing a series of immunity genes that were also repressed during fungal infection. Mutation of sodh-1 in C. elegans blocked ROS accumulation and increased the nematode’s susceptibility to fungal infection. Our study revealed a new recognition and antifungal mechanism in C. elegans. The novel mechanism of ethanol-mediated interaction between the fungus and nematode provides new insights into fungal pathogenesis and for developing alternative biocontrol of pathogenic nematodes by nematophagous fungi. IMPORTANCE Nematodes are among the most abundant animals on our planet. Many of them are parasites in animals and plants and cause human and animal health problems as well as agricultural losses. Studying the interaction of nematodes and their microbial pathogens is of great importance for the biocontrol of animal and plant parasitic nematodes. In this study, we found that the model nematode Caenorhabditis elegans can recognize its fungal pathogen, the nematophagous fungus Purpureocillium lavendulum, through fungal-produced ethanol. Then the nematode elevated the reactive oxygen species production in the gut to inhibit fungal growth in an ethanol dehydrogenase-dependent manner. With this mechanism, novel biocontrol strategies may be developed targeting the ethanol receptor or metabolic pathway of nematodes. Meanwhile, as a volatile organic compound, ethanol should be taken seriously as a vector molecule in the microbial–host interaction in nature.https://journals.asm.org/doi/10.1128/spectrum.01270-23nematophagous fungifungal infectioninnate immunityethanolethanol dehydrogenasepathogen recognition |
| spellingShingle | Xue-Mei Zhuang Zhi-Yi Guo Meng Zhang Yong-Hong Chen Feng-Na Qi Ren-Qiao Wang Ling Zhang Pei-Ji Zhao Chao-Jun Lu Cheng-Gang Zou Yi-Cheng Ma Jianping Xu Ke-Qin Zhang Yan-Ru Cao Lian-Ming Liang Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulum Microbiology Spectrum nematophagous fungi fungal infection innate immunity ethanol ethanol dehydrogenase pathogen recognition |
| title | Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulum |
| title_full | Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulum |
| title_fullStr | Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulum |
| title_full_unstemmed | Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulum |
| title_short | Ethanol mediates the interaction between Caenorhabditis elegans and the nematophagous fungus Purpureocillium lavendulum |
| title_sort | ethanol mediates the interaction between caenorhabditis elegans and the nematophagous fungus purpureocillium lavendulum |
| topic | nematophagous fungi fungal infection innate immunity ethanol ethanol dehydrogenase pathogen recognition |
| url | https://journals.asm.org/doi/10.1128/spectrum.01270-23 |
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