Exploring the specialized metabolome of the plant pathogen Streptomyces sp. 11-1-2

O’Brien, J. & Wright, G. D. An ecological perspective of microbial secondary metabolism. Curr. Opin. Biotechnol. 22, 552–558 (2011).

Article 
PubMed 

Google Scholar 

Scott, J. J. et al. Bacterial protection of beetle-fungus mutualism. Science 1979(322), 63–63 (2008).

Article 
ADS 

Google Scholar 

Oh, D. C., Scott, J. J., Currie, C. R. & Clardy, J. Mycangimycin, a polyene peroxide from a mutualist Streptomyces sp.. Org. Lett. 11, 633–636 (2009).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Kim, D. R. et al. A mutualistic interaction between Streptomyces bacteria, strawberry plants and pollinating bees. Nat. Commun. https://doi.org/10.1038/s41467-019-12785-3 (2019).

Article 
PubMed 
PubMed Central 

Google Scholar 

Traxler, M. F. & Kolter, R. Natural products in soil microbe interactions and evolution. Nat. Prod. Rep. 32, 956–970 (2015).

Article 
CAS 
PubMed 

Google Scholar 

Cornforth, D. M. & Foster, K. R. Competition sensing: The social side of bacterial stress responses. Nat. Rev. Microbiol. 11, 285–293 (2013).

Article 
CAS 
PubMed 

Google Scholar 

Vaz Jauri, P. & Kinkel, L. L. Nutrient overlap, genetic relatedness and spatial origin influence interaction-mediated shifts in inhibitory phenotype among Streptomyces spp.. FEMS Microbiol. Ecol. 90, 264–275 (2014).

Article 
CAS 
PubMed 

Google Scholar 

Lee, N. et al. Mini review: Genome mining approaches for the identification of secondary metabolite biosynthetic gene clusters in Streptomyces. Comput. Struct. Biotechnol. J. 18, 1548–1556 (2020).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Nett, M., Ikeda, H. & Moore, B. S. Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat. Prod. Rep. 26, 1362–1384 (2009).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Hwang, K. S., Kim, H. U., Charusanti, P., Palsson, B. T. & Lee, S. Y. Systems biology and biotechnology of Streptomyces species for the production of secondary metabolites. Biotechnol. Adv. 32, 255–268 (2014).

Article 
CAS 
PubMed 

Google Scholar 

Bode, H. B., Bethe, B., Höfs, R. & Zeeck, A. Big effects from small changes: Possible ways to explore nature’s chemical diversity. ChemBioChem 3, 619–627 (2002).

Article 
CAS 
PubMed 

Google Scholar 

Romano, S., Jackson, S. A., Patry, S. & Dobson, A. D. W. Extending the “one strain many compounds” (OSMAC) principle to marine microorganisms. Mar. Drugs 16, 1–29 (2018).

Article 

Google Scholar 

Terlouw, B. R. et al. MIBiG 3.0: A community-driven effort to annotate experimentally validated biosynthetic gene clusters. Nucleic Acids Res. 51, epub ahead of print (2022).

Blin, K. et al. AntiSMASH 6.0: Improving cluster detection and comparison capabilities. Nucleic Acids Res. 49, W29–W35 (2021).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Bayona, L. M., de Voogd, N. J. & Choi, Y. H. Metabolomics on the study of marine organisms. Metabolomics 18, 1–24 (2022).

Article 

Google Scholar 

van Bergeijk, D. A., Terlouw, B. R., Medema, M. H. & van Wezel, G. P. Ecology and genomics of Actinobacteria: New concepts for natural product discovery. Nat. Rev. Microbiol. 18, 546–558 (2020).

Article 
PubMed 

Google Scholar 

Wu, C., Kim, H. K., Van Wezel, G. P. & Choi, Y. H. Metabolomics in the natural products field—A gateway to novel antibiotics. Drug Discov. Today Technol. 13, 11–17 (2015).

Article 
PubMed 

Google Scholar 

Kind, T. et al. Identification of small molecules using accurate mass MS/MS search. Mass Spectrom. Rev. 37, 513–532 (2018).

Article 
ADS 
CAS 
PubMed 

Google Scholar 

Chaleckis, R., Meister, I., Zhang, P. & Wheelock, C. E. Challenges, progress and promises of metabolite annotation for LC-MS-based metabolomics. Curr. Opin. Biotechnol. 55, 44–50 (2019).

Article 
CAS 
PubMed 

Google Scholar 

Wang, M. et al. Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nat. Biotechnol. 34, 828–837 (2016).

Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Nothias, L. F. et al. Feature-based molecular networking in the GNPS analysis environment. Nat. Methods 17, 905–908 (2020).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Schmid, R. et al. Ion identity molecular networking for mass spectrometry-based metabolomics in the GNPS environment. Nat. Commun. https://doi.org/10.1038/s41467-021-23953-9 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar 

Li, Y., Liu, J., Díaz-Cruz, G., Cheng, Z. & Bignell, D. R. D. Virulence mechanisms of plant-pathogenic Streptomyces species: An updated review. Microbiology 165, 1025–1040 (2019).

Article 
CAS 
PubMed 

Google Scholar 

Cao, Z., Khodakaramian, G., Arakawa, K. & Kinashi, H. Isolation of Borrelidin as a phytotoxic compound from a potato pathogenic Streptomyces strain. Biosci. Biotechnol. Biochem. 76, 353–357 (2012).

Article 
CAS 
PubMed 

Google Scholar 

Lapaz, M. I. et al. Isolation and structural characterization of a non-diketopiperazine phytotoxin from a potato pathogenic Streptomyces strain. Nat. Prod. Res. 0, 1–7 (2018).

Díaz-Cruz, G. A., Liu, J., Tahlan, K. & Bignell, D. R. D. Nigericin and geldanamycin are phytotoxic specialized metabolites produced by the plant pathogen Streptomyces sp. 11-1-2. Microbiol. Spectr. https://doi.org/10.1128/spectrum.02314-21 (2022).

Article 
PubMed 
PubMed Central 

Google Scholar 

Zhu, J. et al. Identification and catalytic characterization of a nonribosomal peptide synthetase-like (NRPS-like) enzyme involved in the biosynthesis of echosides from Streptomyces sp. LZ35. Gene 546, 352–358 (2014).

Article 
CAS 
PubMed 

Google Scholar 

Fyans, J. K., Altowairish, M. S., Li, Y. & Bignell, D. R. D. Characterization of the coronatine-like phytotoxins produced by the common scab pathogen Streptomyces scabies. Mol. Plant Microbe Interact. 28, 443–454 (2015).

Article 
CAS 
PubMed 

Google Scholar 

Johnson, E. G., Joshi, M. V., Gibson, D. M. & Loria, R. Cello-oligosaccharides released from host plants induce pathogenicity in scab-causing Streptomyces species. Physiol. Mol. Plant Pathol. 71, 18–25 (2007).

Article 
CAS 

Google Scholar 

Paradkar, A. S. & Jensen, S. E. Functional analysis of the gene encoding the clavaminate synthase 2 isoenzyme involved in clavulanic acid biosynthesis in Streptomyces clavuligerus. J. Bacteriol. 177, 1307–1314 (1995).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Kieser, T., Bibb, M. J., Buttner, M. J., Chater, K. F. & Hopwood, D. A. Practical Streptomyces Genetics (The John Innes Foundation, 2000).

Google Scholar 

Ikeda, H., Kotaki, H., Tanaka, H. & Omura, S. Involvement of glucose catabolism in avermectin production by Streptomyces avermitilis. Antimicrob. Agents Chemother. 32, 282–284 (1988).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Fyans, J. K., Bown, L. & Bignell, D. R. D. Isolation and characterization of plant pathogenic Streptomyces species associated with common scab-infected potato tubers in Newfoundland. Phytopathology 106, 1–46 (2016).

Article 

Google Scholar 

Celenza, J. L., Grisafi, P. L. & Fink, G. R. A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev. 9, 2131–2142 (1995).

Article 
CAS 
PubMed 

Google Scholar 

Du, Y. & Scheres, B. Lateral root formation and the multiple roles of auxin. J. Exp. Bot. 69, 155–167 (2018).

Article 
CAS 
PubMed 

Google Scholar 

Hayashi, K. I. Chemical biology in auxin research. Cold Spring Harb. Perspect. Biol. https://doi.org/10.1101/cshperspect.a040105 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar 

Stoeckle, D., Thellmann, M. & Vermeer, J. E. Breakout—lateral root emergence in Arabidopsis thaliana. Curr. Opin. Plant Biol. 41, 67–72 (2018).

Article 
PubMed 

Google Scholar 

Staswick, P. E. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol. 150, 1310–1321 (2009).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Yamazoe, A., Hayashi, K. I., Kepinski, S., Leyser, O. & Nozaki, H. Characterization of terfestatin A, a new specific inhibitor for auxin signaling. Plant Physiol. 139, 779–789 (2005).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Hayashi, K.-I. et al. A new inhibitor of auxin signal transduction, from Streptomyces diastatochromogenes B59. J. Antibiot. 54, 573–581 (2001).

Article 
CAS 

Google Scholar 

Hayashi, K. I. et al. A novel inhibitor of auxin action, blocks degradation of AUX/IAA factors. J. Biol. Chem. 278, 23797–23806 (2003).

Article 
CAS 
PubMed 

Google Scholar 

Dührkop, K. et al. SIRIUS 4: A Rapid Tool for Turning Tandem Mass Spectra into Metabolite Structure Information. Nature Methods vol. 16 (Springer, 2019).

Xing, S., Shen, S., Xu, B., Li, X. & Huan, T. BUDDY: Molecular formula discovery via bottom-up MS/MS interrogation. Nat. Methods https://doi.org/10.1038/s41592-023-01850-x (2023).

Article 
PubMed 
PubMed Central 

Google Scholar 

Deng, J. et al. P-Terphenyl O-β-glucuronides, DNA topoisomerase inhibitors from Streptomyces sp. LZ35ΔgdmAI. Bioorg. Med. Chem. Lett. 24, 1362–1365 (2014).

Article 
CAS 
PubMed 

Google Scholar 

Yamazoe, A., Hayashi, K. I., Kuboki, A., Ohira, S. & Nozaki, H. The isolation, structural determination, and total synthesis of terfestatin A, a novel auxin signaling inhibitor from Streptomyces sp.. Tetrahedron Lett. 45, 8359–8362 (2004).

Article 
CAS 

Google Scholar 

Álvarez-Álvarez, R. et al. Molecular genetics of naringenin biosynthesis, a typical plant secondary metabolite produced by Streptomyces clavuligerus. Microb. Cell Fact. 14, 1–12 (2015).

Article 

Google Scholar 

AbuSara, N. F. et al. Comparative genomics and metabolomics analyses of clavulanic acid-producing Streptomyces species provides insight into specialized metabolism. Front. Microbiol. 10, 1–17 (2019).

Article 

Google Scholar 

Shaikh, A. A., Nothias, L. F., Srivastava, S. K., Dorrestein, P. C. & Tahlan, K. Specialized metabolites from ribosome engineered strains of Streptomyces clavuligerus. Metabolites https://doi.org/10.3390/metabo11040239 (2021).

Article 
PubMed 
PubMed Central 

Google Scholar 

Clinger, J. A. et al. Structure and function of a dual reductase-dehydratase enzyme system involved in p-terphenyl biosynthesis. ACS Chem. Biol. 16, 2816–2824 (2021).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Gui, M., Zhang, M.-X., Wen-hui, W. & Sun, P. Natural occurrence, bioactivity and biosynthesis of elaiophylin analogues. Molecules 24(21), 3840. https://doi.org/10.3390/molecules24213840 (2019).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Lee, S. Y. et al. Structure determination and biological activities of elaiophylin produced by Streptomyces sp. MCY-846. J. Microbiol. Biotechnol. 6, 245–249. Preprint at (1996).

Klassen, J. L., Lee, S. R., Poulsen, M., Beemelmanns, C. & Kim, K. H. Efomycins K and L from a termite-associated Streptomyces sp. M56 and their putative biosynthetic origin. Front. Microbiol. 10, 1–8 (2019).

Article 

Google Scholar 

Han, Y. et al. Halichoblelide D, a new elaiophylin derivative with potent cytotoxic activity from mangrove-derived Streptomyces sp. 219807. Molecules 21, 970 (2016).

Article 
PubMed 
PubMed Central 

Google Scholar 

Sheng, Y. et al. Identification of Elaiophylin Skeletal variants from the Indonesian Streptomyces sp. ICBB 9297. J. Nat. Prod. 78, 2768–2775 (2015).

Article 
CAS 
PubMed 

Google Scholar 

Wu, C. et al. Identification of Elaiophylin Derivatives from the Marine-Derived Actinomycete Streptomyces sp. 7-145 using PCR-based screening. J. Nat. Prod. 76, 2153–2157 (2013).

Article 
CAS 
PubMed 

Google Scholar 

Supong, K. et al. Antimicrobial compounds from endophytic Streptomyces sp. BCC72023 isolated from rice (Oryza sativa L.). Res. Microbiol. 167, 290–298 (2016).

Article 
CAS 
PubMed 

Google Scholar 

Burkhardt, K., Fiedler, H.-P., Grabley, S., Thiericke, R. & Zeeck, A. New Cineromycins and Musacins obtained by metabolite pattern analysis of Streptomyces griseoviridis (FH-S 1832). I. Taxonomy, fermentation, isolation and biological activity. J. Antibiot. 49, 432–437 (1996).

Article 
CAS 

Google Scholar 

Schneider, A. et al. New Cineromycins and Musacins obtained by metabolite pattern analysis of Streptomyces griseoviridis FH-S 1832). II. Structure Elucidation. J. Antibiot. 49, 438–446 (1996).

Article 
CAS 

Google Scholar 

Fukushima, T., Tanaka, M., Gohbara, M. & Fujimori, T. Phytotoxicity of three lactones from Nigrospora sacchari. Phytochemistry 48, 625–630 (1998).

Article 
CAS 

Google Scholar 

Ivanova, V., Schlegel, R. & Dornberger, K. N′-methylniphimycin, a novel minor congener of niphimycin from Streptomyces spec. 57-13. J. Basic Microbiol. 38, 415–419 (1998).

Article 
CAS 
PubMed 

Google Scholar 

Chen, Y. et al. Discovery of Niphimycin C from Streptomyces yongxingensis sp. nov. as a promising agrochemical fungicide for controlling banana fusarium wilt by destroying the mitochondrial structure and function. J. Agric. Food Chem. 70, 12784–12795 (2022).

Article 
CAS 
PubMed 

Google Scholar 

Hu, Y. et al. Identification and proposed relative and absolute configurations of Niphimycins C-E from the marine-derived Streptomyces sp. IMB7-145 by genomic analysis. J. Nat. Prod. 81, 178–187 (2018).

Article 
CAS 
PubMed 

Google Scholar 

Usuki, Y. et al. Structure-activity relationship studies on niphimycin, a guanidylpolyol macrolide antibiotic. Part 1: The role of the N-methyl-N″-alkylguanidinium moiety. Bioorg. Med. Chem. Lett. 16, 1553–1556 (2006).

Article 
CAS 
PubMed 

Google Scholar 

Takesako, K. & Beppu, T. Studies on new antifungal antibiotics, guanidylfungins A and B. I. Taxonomy, fermentation, isolation and characterization. J. Antibiot. 37, 1161–1169 (1984).

Article 
CAS 

Google Scholar 

Karki, S. et al. The methoxymalonyl-acyl carrier protein biosynthesis locus and the nearby gene with the β-ketoacyl synthase domain are involved in the biosynthesis of galbonolides in Streptomyces galbus, but these loci are separate from the modular polyketide synt. FEMS Microbiol. Lett. 310, 69–75 (2010).

Article 
CAS 
PubMed 

Google Scholar 

Liu, C., Zhang, J., Lu, C. & Shen, Y. Heterologous expression of galbonolide biosynthetic genes in Streptomyces coelicolor. Antonie van Leeuwenhoek, Int. J. General Mol. Microbiol. 107, 1359–1366 (2015).

Article 
CAS 

Google Scholar 

Zhang, J., Chang, X., Li, Y. & Lu, C. Galbonolides from Streptomyces sp. SR107. Nat. Prod. Commun. 11, 1869–1870 (2016).

PubMed 

Google Scholar 

Salituro, G. M. et al. Meridamycin: A novel nonimmunosuppressive FKBP12 ligand from Streptomyces hygroscopicus. Tetrahedron Lett. 36, 997–1000 (1995).

Article 
CAS 

Google Scholar 

Gollan, P. J., Bhave, M. & Aro, E. M. The FKBP families of higher plants: Exploring the structures and functions of protein interaction specialists. FEBS Lett. 586, 3539–3547 (2012).

Article 
CAS 
PubMed 

Google Scholar 

Xiong, Y. & Sheen, J. The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol. 164, 499–512 (2014).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Xiong, F. et al. Tomato FK506 binding protein 12KD (FKBP12) mediates the interaction between rapamycin and target of rapamycin (TOR). Front. Plant. Sci. https://doi.org/10.3389/fpls.2016.01746 (2016).

Article 
PubMed 
PubMed Central 

Google Scholar 

Montané, M. H. & Menand, B. ATP-competitive mTOR kinase inhibitors delay plant growth by triggering early differentiation of meristematic cells but no developmental patterning change. J. Exp. Bot. 64, 4361–4374 (2013).

Article 
PubMed 
PubMed Central 

Google Scholar 

Liu, M., Lu, C. & Shen, Y. Four new meridamycin congeners from: Streptomyces sp. SR107. RSC Adv. 6, 49792–49796 (2016).

Article 
ADS 
CAS 

Google Scholar 

He, M., Haltli, B., Summers, M., Feng, X. & Hucul, J. Isolation and characterization of meridamycin biosynthetic gene cluster from Streptomyces sp. NRRL 30748. Gene 377, 109–118 (2006).

Article 
CAS 
PubMed 

Google Scholar 

Sun, Y. et al. Organization of the biosynthetic gene cluster in Streptomyces sp. DSM 4137 for the novel neuroprotectant polyketide meridamycin. Microbiology 152, 3507–3515 (2006).

Article 
CAS 
PubMed 

Google Scholar 

Natsume, M., Tashiro, N., Doi, A., Nishi, Y. & Kawaide, H. Effects of concanamycins produced by Streptomyces scabies on lesion type of common scab of potato. J. General Plant Pathol. 83, 78–82 (2017).

Article 
CAS 

Google Scholar 

Igarashi, Y., Iida, T., Yoshida, R. & Furumai, T. Pteridic acids A and B, novel plant growth promoters with auxin-like activity from Streptomyces hygroscopicus TP-A0451. J. Antibiot. 55, 764–767 (2002).

Article 
CAS 

Google Scholar 

Yang, Z. et al. Streptomyces alleviate abiotic stress in plant by producing pteridic acids. bioRxiv 2022.11.18.517137 (2022).

Buell, C. R. et al. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. 100, 10181–10186 (2003).

Article 
ADS 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Russell, D. W. & Sambrook, J. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory, 2001).

Google Scholar 

Chambers, M. C. et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 30, 918–920 (2012).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Pluskal, T., Castillo, S., Villar-Briones, A. & Orešič, M. MZmine 2: Modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinf. 11, 395 (2010).

Article 

Google Scholar 

Shannon, P. et al. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).

Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 

Ruttkies, C., Schymanski, E. L., Wolf, S., Hollender, J. & Neumann, S. MetFrag relaunched: Incorporating strategies beyond in silico fragmentation. J. Cheminform. 8, 1–16 (2016).

Article 

Google Scholar 

Dührkop, K., Shen, H., Meusel, M., Rousu, J. & Böcker, S. Searching molecular structure databases with tandem mass spectra using CSI:FingerID. Proc. Natl. Acad. Sci. USA 112, 12580–12585 (2015).

Article 
ADS 
PubMed 
PubMed Central 

Google Scholar 

Loria, R. et al. Differential production of thaxtomins by pathogenic Streptomyces species in vitro. Phytopathology 85, 537–541 (1995).

Article 
CAS 

Google Scholar 

Blin, K. et al. antiSMASH 7.0: New and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res. https://doi.org/10.1093/nar/gkad344 (2023).

Article 
PubMed 
PubMed Central 

Google Scholar 

Navarro-Muñoz, J. C. et al. A computational framework to explore large-scale biosynthetic diversity. Nat Chem Biol 16, 60–68 (2020).

Article 
PubMed 

Google Scholar 

Gilchrist, C. L. M. & Chooi, Y. H. Clinker & clustermap.js: Automatic generation of gene cluster comparison figures. Bioinformatics 37, 2473–2475 (2021).

Article 
CAS 
PubMed 

Google Scholar 

van den Belt, M. et al. CAGECAT: The CompArative GEne cluster analysis toolbox for rapid search and visualisation of homologous gene clusters. BMC Bioinform. 24, 181 (2023).

Article 

Google Scholar 

Harrison, K. J., Crécy-Lagard, V. D. & Zallot, R. Gene graphics: A genomic neighborhood data visualization web application. Bioinformatics 34, 1406–1408 (2018).

Article 
CAS 
PubMed 

Google Scholar 

de Mendiburu, F. Agricolae: Statistical procedures for agricultural research. Preprint at (2020).

Wickham, H. Ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).

Book 

Google Scholar 

Ahlmann-Eltze, C. ggsignif: Significance Brackets for ‘ggplot2’. Preprint at (2019).

Pedersen, T. L. Patchwork: The composer of plots. Preprint at (2020).