Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1
Abstract Actinobacteria are one of the predominant groups that successfully colonize and survive in various aquatic, terrestrial and rhizhospheric ecosystems. Among actinobacteria, Nocardia is one of the most important agricultural and industrial bacteria. Screening and isolation of Nocardia related...
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Nature Portfolio
2024-03-01
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| Series: | Scientific Reports |
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| Online Access: | https://doi.org/10.1038/s41598-024-54095-9 |
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| author | Irina V. Khilyas Maria I. Markelova Liia R. Valeeva Tatiana M. Ivoilova Elena Shagimardanova Alexander V. Laikov Anna A. Elistratova Ekaterina S. Berkutova Guenter Lochnit Margarita R. Sharipova |
| author_facet | Irina V. Khilyas Maria I. Markelova Liia R. Valeeva Tatiana M. Ivoilova Elena Shagimardanova Alexander V. Laikov Anna A. Elistratova Ekaterina S. Berkutova Guenter Lochnit Margarita R. Sharipova |
| author_sort | Irina V. Khilyas |
| collection | DOAJ |
| description | Abstract Actinobacteria are one of the predominant groups that successfully colonize and survive in various aquatic, terrestrial and rhizhospheric ecosystems. Among actinobacteria, Nocardia is one of the most important agricultural and industrial bacteria. Screening and isolation of Nocardia related bacteria from extreme habitats such as endolithic environments are beneficial for practical applications in agricultural and environmental biotechnology. In this work, bioinformatics analysis revealed that a novel strain Nocardia mangyaensis NH1 has the capacity to produce structurally varied bioactive compounds, which encoded by non-ribosomal peptide synthases (NRPS), polyketide synthase (PKS), and post-translationally modified peptides (RiPPs). Among NRPS, five gene clusters have a sequence homology with clusters encoding for siderophore synthesis. We also show that N. mangyaensis NH1 accumulates both catechol- and hydroxamate-type siderophores simultaneously under iron-deficient conditions. Untargeted LC–MS/MS analysis revealed a variety of metabolites, including siderophores, lipopeptides, cyclic peptides, and indole-3-acetic acid (IAA) in the culture medium of N. mangyaensis NH1 grown under iron deficiency. We demonstrate that four CAS (chrome azurol S)-positive fractions display variable affinity to metals, with a high Fe3+ chelating capability. Additionally, three of these fractions exhibit antioxidant activity. A combination of iron scavenging metabolites produced by N. mangyaensis NH1 showed antifungal activity against several plant pathogenic fungi. We have shown that the pure culture of N. mangyaensis NH1 and its metabolites have no adverse impact on Arabidopsis seedlings. The ability of N. mangyaensis NH1 to produce siderophores with antifungal, metal-chelating, and antioxidant properties, when supplemented with phytohormones, has the potential to improve the release of macro- and micronutrients, increase soil fertility, promote plant growth and development, and enable the production of biofertilizers across diverse soil systems. |
| first_indexed | 2024-04-25T01:06:20Z |
| format | Article |
| id | doaj.art-cadfd0f657ed4eef9c0fb1eeb5861efa |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-25T01:06:20Z |
| publishDate | 2024-03-01 |
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| spelling | doaj.art-cadfd0f657ed4eef9c0fb1eeb5861efa2024-03-10T12:12:59ZengNature PortfolioScientific Reports2045-23222024-03-0114111310.1038/s41598-024-54095-9Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1Irina V. Khilyas0Maria I. Markelova1Liia R. Valeeva2Tatiana M. Ivoilova3Elena Shagimardanova4Alexander V. Laikov5Anna A. Elistratova6Ekaterina S. Berkutova7Guenter Lochnit8Margarita R. Sharipova9Institute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversityLaboratory of Multiomics Technologies of Living Systems, Institute Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversityInstitute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversityInstitute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversitySkolkovo Institute of Science and TechnologyLaboratory of Multiomics Technologies of Living Systems, Institute Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversityInstitute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversityInstitute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversityProtein Analytics, Institute of Biochemistry, Faculty of Medicine, Justus Liebig University GiessenInstitute of Fundamental Medicine and Biology, Kazan (Volga Region) Federal UniversityAbstract Actinobacteria are one of the predominant groups that successfully colonize and survive in various aquatic, terrestrial and rhizhospheric ecosystems. Among actinobacteria, Nocardia is one of the most important agricultural and industrial bacteria. Screening and isolation of Nocardia related bacteria from extreme habitats such as endolithic environments are beneficial for practical applications in agricultural and environmental biotechnology. In this work, bioinformatics analysis revealed that a novel strain Nocardia mangyaensis NH1 has the capacity to produce structurally varied bioactive compounds, which encoded by non-ribosomal peptide synthases (NRPS), polyketide synthase (PKS), and post-translationally modified peptides (RiPPs). Among NRPS, five gene clusters have a sequence homology with clusters encoding for siderophore synthesis. We also show that N. mangyaensis NH1 accumulates both catechol- and hydroxamate-type siderophores simultaneously under iron-deficient conditions. Untargeted LC–MS/MS analysis revealed a variety of metabolites, including siderophores, lipopeptides, cyclic peptides, and indole-3-acetic acid (IAA) in the culture medium of N. mangyaensis NH1 grown under iron deficiency. We demonstrate that four CAS (chrome azurol S)-positive fractions display variable affinity to metals, with a high Fe3+ chelating capability. Additionally, three of these fractions exhibit antioxidant activity. A combination of iron scavenging metabolites produced by N. mangyaensis NH1 showed antifungal activity against several plant pathogenic fungi. We have shown that the pure culture of N. mangyaensis NH1 and its metabolites have no adverse impact on Arabidopsis seedlings. The ability of N. mangyaensis NH1 to produce siderophores with antifungal, metal-chelating, and antioxidant properties, when supplemented with phytohormones, has the potential to improve the release of macro- and micronutrients, increase soil fertility, promote plant growth and development, and enable the production of biofertilizers across diverse soil systems.https://doi.org/10.1038/s41598-024-54095-9Endolithic bacteriaNocardiaSiderophoresMetabolomeNRPSAntifungal activity |
| spellingShingle | Irina V. Khilyas Maria I. Markelova Liia R. Valeeva Tatiana M. Ivoilova Elena Shagimardanova Alexander V. Laikov Anna A. Elistratova Ekaterina S. Berkutova Guenter Lochnit Margarita R. Sharipova Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1 Scientific Reports Endolithic bacteria Nocardia Siderophores Metabolome NRPS Antifungal activity |
| title | Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1 |
| title_full | Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1 |
| title_fullStr | Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1 |
| title_full_unstemmed | Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1 |
| title_short | Genomic insights and anti-phytopathogenic potential of siderophore metabolome of endolithic Nocardia mangyaensis NH1 |
| title_sort | genomic insights and anti phytopathogenic potential of siderophore metabolome of endolithic nocardia mangyaensis nh1 |
| topic | Endolithic bacteria Nocardia Siderophores Metabolome NRPS Antifungal activity |
| url | https://doi.org/10.1038/s41598-024-54095-9 |
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