Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinum
Volatile organic compounds (VOCs) play an important role in the communication among organisms, including plants, beneficial or pathogenic microbes, and pests. In vitro, we observed that the growth of seven out of eight Basidiomycete species tested was inhibited by the VOCs of the biocontrol agent Ps...
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Frontiers Media S.A.
2021-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.684664/full |
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| author | Maria Isabella Prigigallo Angelo De Stradis Abhishek Anand Francesco Mannerucci Floriane L’Haridon Laure Weisskopf Giovanni Bubici |
| author_facet | Maria Isabella Prigigallo Angelo De Stradis Abhishek Anand Francesco Mannerucci Floriane L’Haridon Laure Weisskopf Giovanni Bubici |
| author_sort | Maria Isabella Prigigallo |
| collection | DOAJ |
| description | Volatile organic compounds (VOCs) play an important role in the communication among organisms, including plants, beneficial or pathogenic microbes, and pests. In vitro, we observed that the growth of seven out of eight Basidiomycete species tested was inhibited by the VOCs of the biocontrol agent Pseudomonas protegens strain CHA0. In the Ascomycota phylum, only some species were sensitive (e.g., Sclerotinia sclerotiorum, Botrytis cinerea, etc.) but others were resistant (e.g., Fusarium oxysporum f. sp. cubense, Verticillium dahliae, etc.). We further discovered that CHA0 as well as other ten beneficial or phytopathogenic bacterial strains were all able to inhibit Heterobasidion abietinum, which was used in this research as a model species. Moreover, such an inhibition occurred only when bacteria grew on media containing digested proteins like peptone or tryptone (e.g., Luria-Bertani agar or LBA). Also, the inhibition co-occurred with a pH increase of the agar medium where the fungus grew. Therefore, biogenic ammonia originating from protein degradation by bacteria was hypothesized to play a major role in fungus inhibition. Indeed, when tested as a synthetic compound, it was highly toxic to H. abietinum (effective concentration 50% or EC50 = 1.18 M; minimum inhibitory concentration or MIC = 2.14 M). Using gas chromatography coupled to mass spectrometry (GC/MS), eight VOCs were found specifically emitted by CHA0 grown on LBA compared to the bacterium grown on potato dextrose agar (PDA). Among them, two compounds were even more toxic than ammonia against H. abietinum: dimethyl trisulfide had EC50 = 0.02 M and MIC = 0.2 M, and 2-ethylhexanol had EC50 = 0.33 M and MIC = 0.77 M. The fungus growth inhibition was the result of severe cellular and sub-cellular alterations of hyphae occurring as early as 15 min of exposure to VOCs, as evidenced by transmission and scanning electron microscopy observations. Transcriptome reprogramming of H. abietinum induced by CHA0’s VOCs pointed out that detrimental effects occurred on ribosomes and protein synthesis while the cells tried to react by activating defense mechanisms, which required a lot of energy diverted from the growth and development (fitness cost). |
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| language | English |
| last_indexed | 2024-12-17T00:45:41Z |
| publishDate | 2021-05-01 |
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| spelling | doaj.art-e10390fdb06a4cc6bf630f8b982466f72022-12-21T22:09:55ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-05-011210.3389/fmicb.2021.684664684664Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinumMaria Isabella Prigigallo0Angelo De Stradis1Abhishek Anand2Francesco Mannerucci3Floriane L’Haridon4Laure Weisskopf5Giovanni Bubici6Istituto per la Protezione Sostenibile delle Piante, Consiglio Nazionale delle Ricerche, Bari, ItalyIstituto per la Protezione Sostenibile delle Piante, Consiglio Nazionale delle Ricerche, Bari, ItalyDepartment of Biology, University of Fribourg, Fribourg, SwitzerlandDipartimento di Scienze del Suolo, della Pianta e degli Alimenti, Università degli Studi di Bari Aldo Moro, Bari, ItalyDepartment of Biology, University of Fribourg, Fribourg, SwitzerlandDepartment of Biology, University of Fribourg, Fribourg, SwitzerlandIstituto per la Protezione Sostenibile delle Piante, Consiglio Nazionale delle Ricerche, Bari, ItalyVolatile organic compounds (VOCs) play an important role in the communication among organisms, including plants, beneficial or pathogenic microbes, and pests. In vitro, we observed that the growth of seven out of eight Basidiomycete species tested was inhibited by the VOCs of the biocontrol agent Pseudomonas protegens strain CHA0. In the Ascomycota phylum, only some species were sensitive (e.g., Sclerotinia sclerotiorum, Botrytis cinerea, etc.) but others were resistant (e.g., Fusarium oxysporum f. sp. cubense, Verticillium dahliae, etc.). We further discovered that CHA0 as well as other ten beneficial or phytopathogenic bacterial strains were all able to inhibit Heterobasidion abietinum, which was used in this research as a model species. Moreover, such an inhibition occurred only when bacteria grew on media containing digested proteins like peptone or tryptone (e.g., Luria-Bertani agar or LBA). Also, the inhibition co-occurred with a pH increase of the agar medium where the fungus grew. Therefore, biogenic ammonia originating from protein degradation by bacteria was hypothesized to play a major role in fungus inhibition. Indeed, when tested as a synthetic compound, it was highly toxic to H. abietinum (effective concentration 50% or EC50 = 1.18 M; minimum inhibitory concentration or MIC = 2.14 M). Using gas chromatography coupled to mass spectrometry (GC/MS), eight VOCs were found specifically emitted by CHA0 grown on LBA compared to the bacterium grown on potato dextrose agar (PDA). Among them, two compounds were even more toxic than ammonia against H. abietinum: dimethyl trisulfide had EC50 = 0.02 M and MIC = 0.2 M, and 2-ethylhexanol had EC50 = 0.33 M and MIC = 0.77 M. The fungus growth inhibition was the result of severe cellular and sub-cellular alterations of hyphae occurring as early as 15 min of exposure to VOCs, as evidenced by transmission and scanning electron microscopy observations. Transcriptome reprogramming of H. abietinum induced by CHA0’s VOCs pointed out that detrimental effects occurred on ribosomes and protein synthesis while the cells tried to react by activating defense mechanisms, which required a lot of energy diverted from the growth and development (fitness cost).https://www.frontiersin.org/articles/10.3389/fmicb.2021.684664/fullHeterobasidionPseudomonasvolatile organic compounds (VOCs)biological control agentsbiocontrolmicrobe–microbe interaction |
| spellingShingle | Maria Isabella Prigigallo Angelo De Stradis Abhishek Anand Francesco Mannerucci Floriane L’Haridon Laure Weisskopf Giovanni Bubici Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinum Frontiers in Microbiology Heterobasidion Pseudomonas volatile organic compounds (VOCs) biological control agents biocontrol microbe–microbe interaction |
| title | Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinum |
| title_full | Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinum |
| title_fullStr | Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinum |
| title_full_unstemmed | Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinum |
| title_short | Basidiomycetes Are Particularly Sensitive to Bacterial Volatile Compounds: Mechanistic Insight Into the Case Study of Pseudomonas protegens Volatilome Against Heterobasidion abietinum |
| title_sort | basidiomycetes are particularly sensitive to bacterial volatile compounds mechanistic insight into the case study of pseudomonas protegens volatilome against heterobasidion abietinum |
| topic | Heterobasidion Pseudomonas volatile organic compounds (VOCs) biological control agents biocontrol microbe–microbe interaction |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.684664/full |
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