Lipopeptides as rhizosphere public goods for microbial cooperation
ABSTRACT Cyclic lipopeptides (CLPs) are key bioactive secondary metabolites produced by some plant beneficial rhizobacteria such as Pseudomonas and Bacillus. They exhibit antimicrobial properties, promote induced systemic resistance in plants, and support key developmental traits, including motility...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-01-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.03106-23 |
| _version_ | 1827383642744160256 |
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| author | Augustin Rigolet Anthony Argüelles Arias Adrien Anckaert Loïc Quinton Sébastien Rigali Deborah Tellatin Pierre Burguet Marc Ongena |
| author_facet | Augustin Rigolet Anthony Argüelles Arias Adrien Anckaert Loïc Quinton Sébastien Rigali Deborah Tellatin Pierre Burguet Marc Ongena |
| author_sort | Augustin Rigolet |
| collection | DOAJ |
| description | ABSTRACT Cyclic lipopeptides (CLPs) are key bioactive secondary metabolites produced by some plant beneficial rhizobacteria such as Pseudomonas and Bacillus. They exhibit antimicrobial properties, promote induced systemic resistance in plants, and support key developmental traits, including motility, biofilm formation, and root colonization. However, our knowledge about the fate of lipopeptides once released in the environment and especially upon contact with neighboring rhizobacteria remains limited. Here, we investigated the enzymatic degradation of Bacillus and Pseudomonas cyclic lipopeptides by Streptomyces. We observed that Streptomyces venezuelae is able to degrade the three lipopeptides surfactin, iturin, and fengycin upon interaction with Bacillus velezensis in vitro and in planta according to specific mechanisms. S. venezuelae was also able to degrade the structurally diverse sessilin-, tolaasin-, orfamide-, xantholisin-, and putisolvin-type lipopeptides produced by Pseudomonas, indicating that this trait is likely engaged in the interaction with various competitors. Furthermore, the degradation of CLPs is associated with the release of free amino and fatty acids used by Streptomyces to sustain growth. Additionally, we hypothesize that lipopeptide-producing rhizobacteria and their biocontrol potential are impacted by the degradation of their lipopeptides as observed with the polarized motility of B. velezensis, avoiding the confrontation zone with Streptomyces and the loss of antifungal properties of degraded iturin. IMPORTANCE Here, we provide new insights into the possible fate of cyclic lipopeptides as prominent specialized metabolites from beneficial bacilli and pseudomonads once released in the soil. Our data illustrate how the B. velezensis lipopeptidome may be enzymatically remodeled by Streptomyces as important members of the soil bacterial community. The enzymatic arsenal of S. venezuelae enables an unsuspected extensive degradation of these compounds, allowing the bacterium to feed on these exogenous products via a mechanism going beyond linearization, which was previously reported as a detoxification strategy. As soils are carbon-rich and nitrogen-poor environments, we propose a new role for cyclic lipopeptides in interspecies interactions, which is to fuel the nitrogen metabolism of a part of the rhizosphere microbial community. Streptomyces and other actinomycetes, producing numerous peptidases and displaying several traits of beneficial bacteria, should be at the front line to directly benefit from these metabolites as “public goods” for microbial cooperation. |
| first_indexed | 2024-03-08T14:44:19Z |
| format | Article |
| id | doaj.art-bea88efb183345808e03e7dc968af1f1 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-08T14:44:19Z |
| publishDate | 2024-01-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-bea88efb183345808e03e7dc968af1f12024-01-11T14:04:37ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-01-0112110.1128/spectrum.03106-23Lipopeptides as rhizosphere public goods for microbial cooperationAugustin Rigolet0Anthony Argüelles Arias1Adrien Anckaert2Loïc Quinton3Sébastien Rigali4Deborah Tellatin5Pierre Burguet6Marc Ongena7Microbial Processes and Interactions laboratory, TERRA teaching and research centre, Gembloux Agro-Bio Tech,University of Liège , Gembloux, BelgiumMicrobial Processes and Interactions laboratory, TERRA teaching and research centre, Gembloux Agro-Bio Tech,University of Liège , Gembloux, BelgiumMicrobial Processes and Interactions laboratory, TERRA teaching and research centre, Gembloux Agro-Bio Tech,University of Liège , Gembloux, BelgiumDepartment of Chemistry, University of Liège , Liège, BelgiumInBioS—Centre for Protein Engineering,University of Liège , Liege, BelgiumInBioS—Centre for Protein Engineering,University of Liège , Liege, BelgiumDepartment of Chemistry, University of Liège , Liège, BelgiumMicrobial Processes and Interactions laboratory, TERRA teaching and research centre, Gembloux Agro-Bio Tech,University of Liège , Gembloux, BelgiumABSTRACT Cyclic lipopeptides (CLPs) are key bioactive secondary metabolites produced by some plant beneficial rhizobacteria such as Pseudomonas and Bacillus. They exhibit antimicrobial properties, promote induced systemic resistance in plants, and support key developmental traits, including motility, biofilm formation, and root colonization. However, our knowledge about the fate of lipopeptides once released in the environment and especially upon contact with neighboring rhizobacteria remains limited. Here, we investigated the enzymatic degradation of Bacillus and Pseudomonas cyclic lipopeptides by Streptomyces. We observed that Streptomyces venezuelae is able to degrade the three lipopeptides surfactin, iturin, and fengycin upon interaction with Bacillus velezensis in vitro and in planta according to specific mechanisms. S. venezuelae was also able to degrade the structurally diverse sessilin-, tolaasin-, orfamide-, xantholisin-, and putisolvin-type lipopeptides produced by Pseudomonas, indicating that this trait is likely engaged in the interaction with various competitors. Furthermore, the degradation of CLPs is associated with the release of free amino and fatty acids used by Streptomyces to sustain growth. Additionally, we hypothesize that lipopeptide-producing rhizobacteria and their biocontrol potential are impacted by the degradation of their lipopeptides as observed with the polarized motility of B. velezensis, avoiding the confrontation zone with Streptomyces and the loss of antifungal properties of degraded iturin. IMPORTANCE Here, we provide new insights into the possible fate of cyclic lipopeptides as prominent specialized metabolites from beneficial bacilli and pseudomonads once released in the soil. Our data illustrate how the B. velezensis lipopeptidome may be enzymatically remodeled by Streptomyces as important members of the soil bacterial community. The enzymatic arsenal of S. venezuelae enables an unsuspected extensive degradation of these compounds, allowing the bacterium to feed on these exogenous products via a mechanism going beyond linearization, which was previously reported as a detoxification strategy. As soils are carbon-rich and nitrogen-poor environments, we propose a new role for cyclic lipopeptides in interspecies interactions, which is to fuel the nitrogen metabolism of a part of the rhizosphere microbial community. Streptomyces and other actinomycetes, producing numerous peptidases and displaying several traits of beneficial bacteria, should be at the front line to directly benefit from these metabolites as “public goods” for microbial cooperation.https://journals.asm.org/doi/10.1128/spectrum.03106-23Bacillus velezensisStreptomyces venezuelaePseudomonasBSMscyclic lipopeptidesenzymatic degradation |
| spellingShingle | Augustin Rigolet Anthony Argüelles Arias Adrien Anckaert Loïc Quinton Sébastien Rigali Deborah Tellatin Pierre Burguet Marc Ongena Lipopeptides as rhizosphere public goods for microbial cooperation Microbiology Spectrum Bacillus velezensis Streptomyces venezuelae Pseudomonas BSMs cyclic lipopeptides enzymatic degradation |
| title | Lipopeptides as rhizosphere public goods for microbial cooperation |
| title_full | Lipopeptides as rhizosphere public goods for microbial cooperation |
| title_fullStr | Lipopeptides as rhizosphere public goods for microbial cooperation |
| title_full_unstemmed | Lipopeptides as rhizosphere public goods for microbial cooperation |
| title_short | Lipopeptides as rhizosphere public goods for microbial cooperation |
| title_sort | lipopeptides as rhizosphere public goods for microbial cooperation |
| topic | Bacillus velezensis Streptomyces venezuelae Pseudomonas BSMs cyclic lipopeptides enzymatic degradation |
| url | https://journals.asm.org/doi/10.1128/spectrum.03106-23 |
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