Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum Chlamydospores
ABSTRACT Strains of the Ralstonia solanacearum species complex (RSSC), although known as the causative agent of bacterial wilt disease in plants, induce the chlamydospores of many fungal species and invade them through the spores. The lipopeptide ralstonins are the chlamydospore inducers produced by...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-08-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00036-23 |
| _version_ | 1828717730152316928 |
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| author | Chiaki Tsumori Shoma Matsuo Yuta Murai Kenji Kai |
| author_facet | Chiaki Tsumori Shoma Matsuo Yuta Murai Kenji Kai |
| author_sort | Chiaki Tsumori |
| collection | DOAJ |
| description | ABSTRACT Strains of the Ralstonia solanacearum species complex (RSSC), although known as the causative agent of bacterial wilt disease in plants, induce the chlamydospores of many fungal species and invade them through the spores. The lipopeptide ralstonins are the chlamydospore inducers produced by RSSC and are essential for this invasion. However, no mechanistic investigation of this interaction has been conducted. In this study, we report that quorum sensing (QS), which is a bacterial cell-cell communication, is important for RSSC to invade the fungus Fusarium oxysporum (Fo). ΔphcB, a deletion mutant of QS signal synthase, lost the ability to both produce ralstonins and invade Fo chlamydospores. The QS signal methyl 3-hydroxymyristate rescued these disabilities. In contrast, exogenous ralstonin A, while inducing Fo chlamydospores, failed to rescue the invasive ability. Gene-deletion and -complementation experiments revealed that the QS-dependent production of extracellular polysaccharide I (EPS I) is essential for this invasion. The RSSC cells adhered to Fo hyphae and formed biofilms there before inducing chlamydospores. This biofilm formation was not observed in the EPS I- or ralstonin-deficient mutant. Microscopic analysis showed that RSSC infection resulted in the death of Fo chlamydospores. Altogether, we report that the RSSC QS system is important for this lethal endoparasitism. Among the factors regulated by the QS system, ralstonins, EPS I, and biofilm are important parasitic factors. IMPORTANCE Ralstonia solanacearum species complex (RSSC) strains infect both plants and fungi. The phc quorum-sensing (QS) system of RSSC is important for parasitism on plants, because it allows them to invade and proliferate within the hosts by causing appropriate activation of the system at each infection step. In this study, we confirm that ralstonin A is important not only for Fusarium oxysporum (Fo) chlamydospore induction but also for RSSC biofilm formation on Fo hyphae. Extracellular polysaccharide I (EPS I) is also essential for biofilm formation, while the phc QS system controls these factors in terms of production. The present results advocate a new QS-dependent mechanism for the process by which a bacterium invades a fungus. |
| first_indexed | 2024-03-12T14:31:42Z |
| format | Article |
| id | doaj.art-ba084faa3e7b42c3be6ecc95c3fc2292 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-12T14:31:42Z |
| publishDate | 2023-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-ba084faa3e7b42c3be6ecc95c3fc22922023-08-17T13:04:13ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-08-0111410.1128/spectrum.00036-23Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum ChlamydosporesChiaki Tsumori0Shoma Matsuo1Yuta Murai2Kenji Kai3Graduate School of Agriculture, Osaka Metropolitan University, Osaka, JapanGraduate School of Agriculture, Osaka Metropolitan University, Osaka, JapanGraduate School of Agriculture, Osaka Metropolitan University, Osaka, JapanGraduate School of Agriculture, Osaka Metropolitan University, Osaka, JapanABSTRACT Strains of the Ralstonia solanacearum species complex (RSSC), although known as the causative agent of bacterial wilt disease in plants, induce the chlamydospores of many fungal species and invade them through the spores. The lipopeptide ralstonins are the chlamydospore inducers produced by RSSC and are essential for this invasion. However, no mechanistic investigation of this interaction has been conducted. In this study, we report that quorum sensing (QS), which is a bacterial cell-cell communication, is important for RSSC to invade the fungus Fusarium oxysporum (Fo). ΔphcB, a deletion mutant of QS signal synthase, lost the ability to both produce ralstonins and invade Fo chlamydospores. The QS signal methyl 3-hydroxymyristate rescued these disabilities. In contrast, exogenous ralstonin A, while inducing Fo chlamydospores, failed to rescue the invasive ability. Gene-deletion and -complementation experiments revealed that the QS-dependent production of extracellular polysaccharide I (EPS I) is essential for this invasion. The RSSC cells adhered to Fo hyphae and formed biofilms there before inducing chlamydospores. This biofilm formation was not observed in the EPS I- or ralstonin-deficient mutant. Microscopic analysis showed that RSSC infection resulted in the death of Fo chlamydospores. Altogether, we report that the RSSC QS system is important for this lethal endoparasitism. Among the factors regulated by the QS system, ralstonins, EPS I, and biofilm are important parasitic factors. IMPORTANCE Ralstonia solanacearum species complex (RSSC) strains infect both plants and fungi. The phc quorum-sensing (QS) system of RSSC is important for parasitism on plants, because it allows them to invade and proliferate within the hosts by causing appropriate activation of the system at each infection step. In this study, we confirm that ralstonin A is important not only for Fusarium oxysporum (Fo) chlamydospore induction but also for RSSC biofilm formation on Fo hyphae. Extracellular polysaccharide I (EPS I) is also essential for biofilm formation, while the phc QS system controls these factors in terms of production. The present results advocate a new QS-dependent mechanism for the process by which a bacterium invades a fungus.https://journals.asm.org/doi/10.1128/spectrum.00036-23Fusarium oxysporumRalstonia solanacearumendoparasitismquorum sensing |
| spellingShingle | Chiaki Tsumori Shoma Matsuo Yuta Murai Kenji Kai Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum Chlamydospores Microbiology Spectrum Fusarium oxysporum Ralstonia solanacearum endoparasitism quorum sensing |
| title | Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum Chlamydospores |
| title_full | Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum Chlamydospores |
| title_fullStr | Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum Chlamydospores |
| title_full_unstemmed | Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum Chlamydospores |
| title_short | Quorum Sensing-Dependent Invasion of Ralstonia solanacearum into Fusarium oxysporum Chlamydospores |
| title_sort | quorum sensing dependent invasion of ralstonia solanacearum into fusarium oxysporum chlamydospores |
| topic | Fusarium oxysporum Ralstonia solanacearum endoparasitism quorum sensing |
| url | https://journals.asm.org/doi/10.1128/spectrum.00036-23 |
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