Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth
ABSTRACT Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about th...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-12-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.01052-22 |
| _version_ | 1798004584544731136 |
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| author | Tomás A. Rush Joanna Tannous Matthew J. Lane Muralikrishnan Gopalakrishnan Meena Alyssa A. Carrell Jacob J. Golan Milton T. Drott Sylvain Cottaz Sébastien Fort Jean-Michel Ané Nancy P. Keller Dale A. Pelletier Daniel A. Jacobson David Kainer Paul E. Abraham Richard J. Giannone Jesse L. Labbé |
| author_facet | Tomás A. Rush Joanna Tannous Matthew J. Lane Muralikrishnan Gopalakrishnan Meena Alyssa A. Carrell Jacob J. Golan Milton T. Drott Sylvain Cottaz Sébastien Fort Jean-Michel Ané Nancy P. Keller Dale A. Pelletier Daniel A. Jacobson David Kainer Paul E. Abraham Richard J. Giannone Jesse L. Labbé |
| author_sort | Tomás A. Rush |
| collection | DOAJ |
| description | ABSTRACT Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition. IMPORTANCE The activation of silent biosynthetic gene clusters (BGC) for the identification and characterization of novel fungal secondary metabolites is a perpetual motion in natural product discoveries. Here, we demonstrated that one of the best-studied symbiosis signaling compounds, lipo-chitooligosaccharides (LCOs), play a role in activating some of these BGCs, resulting in the production of known, putative, and unknown metabolites with biological activities. This collection of metabolites induced by LCOs differentially modulate bacterial growth, while the LCO standards do not convey the same effect. These findings create a paradigm shift showing that LCOs have a more prominent role outside of host recognition of symbiotic microbes. Importantly, our work demonstrates that fungi use LCOs to produce a variety of metabolites with biological activity, which can be a potential source of bio-stimulants, pesticides, or pharmaceuticals. |
| first_indexed | 2024-04-11T12:27:06Z |
| format | Article |
| id | doaj.art-8766e1bbc029479ab06b0e6231809d20 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-11T12:27:06Z |
| publishDate | 2022-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-8766e1bbc029479ab06b0e6231809d202022-12-22T04:23:55ZengAmerican Society for MicrobiologymSystems2379-50772022-12-017610.1128/msystems.01052-22Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial GrowthTomás A. Rush0Joanna Tannous1Matthew J. Lane2Muralikrishnan Gopalakrishnan Meena3Alyssa A. Carrell4Jacob J. Golan5Milton T. Drott6Sylvain Cottaz7Sébastien Fort8Jean-Michel Ané9Nancy P. Keller10Dale A. Pelletier11Daniel A. Jacobson12David Kainer13Paul E. Abraham14Richard J. Giannone15Jesse L. Labbé16Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABredesen Center for Interdisciplinary Research and Graduate Education, University of Tennessee, Knoxville, Tennessee, USANational Center for Computational Sciences, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USADepartment of Botany, University of Wisconsin-Madison, Madison, Wisconsin, USADepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USAUniversité Grenoble Alpes, CNRS, CERMAV, Grenoble, FranceUniversité Grenoble Alpes, CNRS, CERMAV, Grenoble, FranceDepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USADepartment of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USABiosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USAABSTRACT Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition. IMPORTANCE The activation of silent biosynthetic gene clusters (BGC) for the identification and characterization of novel fungal secondary metabolites is a perpetual motion in natural product discoveries. Here, we demonstrated that one of the best-studied symbiosis signaling compounds, lipo-chitooligosaccharides (LCOs), play a role in activating some of these BGCs, resulting in the production of known, putative, and unknown metabolites with biological activities. This collection of metabolites induced by LCOs differentially modulate bacterial growth, while the LCO standards do not convey the same effect. These findings create a paradigm shift showing that LCOs have a more prominent role outside of host recognition of symbiotic microbes. Importantly, our work demonstrates that fungi use LCOs to produce a variety of metabolites with biological activity, which can be a potential source of bio-stimulants, pesticides, or pharmaceuticals.https://journals.asm.org/doi/10.1128/msystems.01052-22lipo-chitooligosaccharidessecondary metabolitessynergismbiosynthetic gene clustersbacteriaAspergillus |
| spellingShingle | Tomás A. Rush Joanna Tannous Matthew J. Lane Muralikrishnan Gopalakrishnan Meena Alyssa A. Carrell Jacob J. Golan Milton T. Drott Sylvain Cottaz Sébastien Fort Jean-Michel Ané Nancy P. Keller Dale A. Pelletier Daniel A. Jacobson David Kainer Paul E. Abraham Richard J. Giannone Jesse L. Labbé Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth mSystems lipo-chitooligosaccharides secondary metabolites synergism biosynthetic gene clusters bacteria Aspergillus |
| title | Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth |
| title_full | Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth |
| title_fullStr | Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth |
| title_full_unstemmed | Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth |
| title_short | Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth |
| title_sort | lipo chitooligosaccharides induce specialized fungal metabolite profiles that modulate bacterial growth |
| topic | lipo-chitooligosaccharides secondary metabolites synergism biosynthetic gene clusters bacteria Aspergillus |
| url | https://journals.asm.org/doi/10.1128/msystems.01052-22 |
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