{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T18:58:08Z","timestamp":1788980288660,"version":"build-2803163510"},"reference-count":57,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,5,31]],"date-time":"2022-05-31T00:00:00Z","timestamp":1653955200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31900030"],"award-info":[{"award-number":["31900030"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p>\n                    <jats:italic>Streptomyces lydicus<\/jats:italic>\n                    was used as biopesticide for crop protection in agriculture, however, the antimicrobial mechanism remains unclear and no systematic research on the secondary metabolites of\n                    <jats:italic>S. lydicus<\/jats:italic>\n                    has been reported. In this study, the extract of\n                    <jats:italic>S. lydicus<\/jats:italic>\n                    M01 culture was used to treat plant pathogen\n                    <jats:italic>Alternaria alternata<\/jats:italic>\n                    and morphological changes in the plasma membrane and cell wall of hyphae and conidia were observed. Fluorescence microscopy combined with different dyes showed that the accumulation of reactive oxygen species and cell death were also induced. To investigate the secondary metabolites in the culture filtrate, an online detection strategy of ultra-high-performance liquid chromatography connected to a quadrupole time-of-flight mass spectrometer (UPLC-Q-TOF-MS) was used for identification. The results revealed an excess of 120 metabolites, mainly consisted of fungicides, antibacterial agents, herbicides, insecticides, and plant growth regulators, such as IAA. Among which the five dominant components were oxadixyl, chloreturon, S-metolachlor, fentrazamide, and bucarpolate. On the other hand, the complete genome of\n                    <jats:italic>S. lydicus<\/jats:italic>\n                    M01 was sequenced and a number of key function gene clusters that contribute to the biosynthesis of active secondary metabolites were revealed. This is the first systematic characterization of\n                    <jats:italic>S. lydicus<\/jats:italic>\n                    secondary metabolites, and these results offer novel and valuable evidence for a comprehensive understanding of the biocontrol agent\n                    <jats:italic>S. lydicus<\/jats:italic>\n                    and its application in agriculture.\n                  <\/jats:p>","DOI":"10.3389\/fmicb.2022.908879","type":"journal-article","created":{"date-parts":[[2022,5,31]],"date-time":"2022-05-31T03:59:20Z","timestamp":1653969560000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":13,"title":["Antimicrobial Mechanism and Secondary Metabolite Profiles of Biocontrol Agent Streptomyces lydicus M01 Based on Ultra-High-Performance Liquid Chromatography Connected to a Quadrupole Time-of-Flight Mass Spectrometer Analysis and Genome Sequencing"],"prefix":"10.3389","volume":"13","author":[{"given":"Mingxuan","family":"Wang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenjie","family":"Cong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jianguo","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,5,31]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.tim.2005.01.007","article-title":"Reactive oxygen species and development in microbial eukaryotes.","volume":"13","author":"Aguirre","year":"2005","journal-title":"Trends Microbiol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1007\/s10295-013-1389-9","article-title":"Microbial genome mining for accelerated natural products discovery: is a renaissance in the making?","volume":"41","author":"Bachmann","year":"2014","journal-title":"J. Ind. Microbiol. Biotechnol."},{"key":"B3","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1038\/417141a","article-title":"Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2).","volume":"417","author":"Bentley","year":"2002","journal-title":"Nature"},{"key":"B4","doi-asserted-by":"publisher","first-page":"1355","DOI":"10.1042\/BST20130214","article-title":"Understanding and manipulating antibiotic production in actinomycetes.","volume":"41","author":"Bibb","year":"2013","journal-title":"Biochem. Soc. Trans."},{"key":"B5","doi-asserted-by":"publisher","first-page":"W29","DOI":"10.1093\/nar\/gkab335","article-title":"antiSMASH 6.0: improving cluster detection and comparison capabilities.","volume":"49","author":"Blin","year":"2021","journal-title":"Nucl. Acids Res."},{"key":"B6","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/0097-8485(93)85004-V","article-title":"GENMARK: parallel gene recognition for both DNA strands.","volume":"17","author":"Borodovsky","year":"1993","journal-title":"Comput. Chem."},{"key":"B7","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.fgb.2010.04.004","article-title":"Fungal secondary metabolites \u2013 Strategies to activate silent gene clusters.","volume":"48","author":"Brakhage","year":"2011","journal-title":"Fungal Genet. Biol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.cbi.2011.01.010","article-title":"ROS-Ca2+ is associated with mitochondria permeability transition pore involved in surfactin-induced MCF-7 cells apoptosis.","volume":"190","author":"Cao","year":"2011","journal-title":"Chem. Biol. Interact."},{"key":"B9","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1038\/ja.2013.25","article-title":"Towards a new science of secondary metabolism.","volume":"66","author":"Craney","year":"2013","journal-title":"J. Antibiot."},{"key":"B10","first-page":"88","article-title":"Discovery, development, and commercialization of a microbial antifungal biocontrol agent, Streptomyces lydicus WYEC108: history of a decade long endeavor.","volume":"55","author":"Crawford","year":"2005","journal-title":"Soc. Ind. Microbiol. News"},{"key":"B11","doi-asserted-by":"publisher","first-page":"3899","DOI":"10.1128\/aem.59.11.3899-3905.1993","article-title":"Isolation and characterization of actinomycete antagonists of a fungal root pathogen.","volume":"59","author":"Crawford Don","year":"1993","journal-title":"Appl. Environ. Microbiol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"673","DOI":"10.1093\/bioinformatics\/btm009","article-title":"Identifying bacterial genes and endosymbiont DNA with Glimmer.","volume":"23","author":"Delcher","year":"2007","journal-title":"Bioinformatics"},{"key":"B13","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.ijmm.2013.09.003","article-title":"Lantibiotics: promising candidates for future applications in health care.","volume":"304","author":"Dischinger","year":"2014","journal-title":"Int. J. Med. Microbiol. Suppl."},{"key":"B14","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1111\/wre.12153","article-title":"Classification of herbicides according to chemical family for weed resistance management strategies \u2013 an update.","volume":"55","author":"Forouzesh","year":"2015","journal-title":"Weed Res."},{"key":"B15","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.foodcont.2013.07.034","article-title":"Identification of bacillomycin D from Bacillus subtilis fmbJ and its inhibition effects against Aspergillus flavus.","volume":"36","author":"Gong","year":"2014","journal-title":"Food Control"},{"key":"B16","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/s0021-9673(02)00083-3","article-title":"Quantification of veterinary antibiotics (sulfonamides and trimethoprim) in animal manure by liquid chromatography\u2013mass spectrometry.","volume":"952","author":"Haller","year":"2002","journal-title":"J. Chromatogr. A"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1166","DOI":"10.1111\/1462-2920.12538","article-title":"The bacterial lipopeptide iturins induce Verticillium dahliae cell death by affecting fungal signalling pathways and mediate plant defence responses involved in pathogen-associated molecular pattern-triggered immunity.","volume":"17","author":"Han","year":"2015","journal-title":"Environ. Microbiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1007\/s00249-006-0091-5","article-title":"Leakage and lysis of lipid membranes induced by the lipopeptide surfactin.","volume":"36","author":"Heerklotz","year":"2007","journal-title":"Eur. Biophys. J."},{"key":"B19","first-page":"249","article-title":"Effects of raised beds, black soil mulch and oxadixyl on root rot (Phytophthora fragariae var. rubi) in red raspberry.","volume":"505","author":"Heiberg","year":"1998","journal-title":"Acta Hortic."},{"key":"B20","doi-asserted-by":"publisher","first-page":"917","DOI":"10.1248\/bpb.34.917","article-title":"Inhibitory effect of cyclic trihydroxamate siderophore, desferrioxamine E, on the biofilm formation of Mycobacterium species.","volume":"34","author":"Ishida","year":"2011","journal-title":"Biol. Pharm. Bull."},{"key":"B21","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1111\/j.1439-0434.1991.tb00102.x","article-title":"Cellular damage to phytophthora infestans in tomato leaves treated with oxadixyl: an ultrastructural investigation.","volume":"132","author":"Jiang","year":"1991","journal-title":"J. Phytopathol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1177\/33.1.2578146","article-title":"An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide.","volume":"33","author":"Jones","year":"1985","journal-title":"J. Histochem. Cytochem."},{"key":"B23","doi-asserted-by":"publisher","first-page":"E753","DOI":"10.1073\/pnas.1715954115","article-title":"Linking secondary metabolites to gene clusters through genome sequencing of six diverse Aspergillus species.","volume":"115","author":"Kj\u00e6rb\u00f8lling","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B24","doi-asserted-by":"publisher","first-page":"11448","DOI":"10.1073\/pnas.0404220101","article-title":"The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor.","volume":"101","author":"Kodani","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1016\/j.micres.2021.126901","article-title":"Rhizospheric microbiome: bio-based emerging strategies for sustainable agriculture development and future perspectives.","volume":"254","author":"Kumawat","year":"2022","journal-title":"Microbiol. Res."},{"key":"B26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1006\/excr.2002.5537","article-title":"Nuclear apoptosis detection by flow cytometry: influence of endogenous endonucleases.","volume":"277","author":"Lecoeur","year":"2002","journal-title":"Exp. Cell Res."},{"key":"B27","first-page":"1050","article-title":"An international database for pesticide risk assessments and management. Human and Ecological Risk Assessment.","volume":"22","author":"Lewis","year":"2016","journal-title":"Int. J."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1294","DOI":"10.1002\/ps.1632","article-title":"Malayamycin, a new streptomycete antifungal compound, specifically inhibits sporulation of Stagonospora nodorum (Berk) Castell and Germano, the cause of wheat glume blotch disease.","volume":"64","author":"Li","year":"2008","journal-title":"Pest Manag. Sci."},{"key":"B29","doi-asserted-by":"publisher","first-page":"311","DOI":"10.3852\/09-176","article-title":"Farnesol induces apoptosis and oxidative stress in the fungal pathogen Penicillium expansum.","volume":"102","author":"Liu","year":"2010","journal-title":"Mycologia"},{"key":"B30","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1007\/s10482-011-9671-1","article-title":"Systematics-guided bioprospecting for bioactive microbial natural products.","volume":"101","author":"Liu","year":"2012","journal-title":"Antonie Van Leeuwenhoek"},{"key":"B31","doi-asserted-by":"publisher","first-page":"2167","DOI":"10.1128\/AAC.01545-05","article-title":"Biosynthetic pathway for mannopeptimycins, lipoglycopeptide antibiotics active against drug-resistant gram-positive pathogens.","volume":"50","author":"Magarvey","year":"2006","journal-title":"Antimicrob Agents Chemother"},{"key":"B32","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/S0141-0229(96)00175-5","article-title":"Properties of the chitinase of the antifungal biocontrol agent Streptomyces lydicus WYEC108.","volume":"20","author":"Mahadevan","year":"1997","journal-title":"Enzyme Microb. Technol."},{"key":"B33","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3209\/saj.20.1","article-title":"An endophytic actinomycete, Streptomyces sp. MBR-52, that accelerates emergence and elongation of plant adventitious roots.","volume":"20","author":"Meguro","year":"2006","journal-title":"Actinomycetologica"},{"key":"B34","doi-asserted-by":"publisher","first-page":"6627","DOI":"10.1128\/AAC.03570-14","article-title":"The production of reactive oxygen species is a universal action mechanism of amphotericin B against pathogenic yeasts and contributes to the fungicidal effect of this drug.","volume":"58","author":"Mesa-Arango Ana","year":"2014","journal-title":"Antimicrob Agents Chemother"},{"key":"B35","doi-asserted-by":"publisher","first-page":"5300","DOI":"10.1016\/j.bmc.2011.08.010","article-title":"Antifungal thiopeptide cyclothiazomycin B1 exhibits growth inhibition accompanying morphological changes via binding to fungal cell wall chitin.","volume":"19","author":"Mizuhara","year":"2011","journal-title":"Bioorg. Med. Chem."},{"key":"B36","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1007\/s00284-005-0412-4","article-title":"Purification, Characterization, and Antifungal Activity of chitinase from Streptomyces venezuelae P10.","volume":"53","author":"Mukherjee","year":"2006","journal-title":"Curr. Microbiol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"12215","DOI":"10.1073\/pnas.211433198","article-title":"Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites.","volume":"98","author":"Omura","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B38","doi-asserted-by":"publisher","first-page":"9621","DOI":"10.1007\/s00253-013-5206-1","article-title":"Effects of actinobacteria on plant disease suppression and growth promotion.","volume":"97","author":"Palaniyandi","year":"2013","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"B39","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1146\/annurev-phyto-082712-102340","article-title":"Induced systemic resistance by beneficial microbes.","volume":"52","author":"Pieterse","year":"2014","journal-title":"Annu. Rev. Phytopathol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"3130","DOI":"10.1128\/AEM.70.5.3130-3132.2004","article-title":"Functional expression of the ectoine hydroxylase gene (thpD) from Streptomyces chrysomallus in Halomonas elongata.","volume":"70","author":"Prabhu","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"1978","DOI":"10.1016\/j.peptides.2010.08.003","article-title":"Lipopeptide induces apoptosis in fungal cells by a mitochondria-dependent pathway.","volume":"31","author":"Qi","year":"2010","journal-title":"Peptides"},{"key":"B42","article-title":"Induced systemic resistance in cucumber and tomato against cucumber mosaic cucumovirus using plant growth-promoting rhizobacteria (PGPR).","volume":"80","author":"Raupach","year":"1996"},{"key":"B43","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.tplants.2016.10.008","article-title":"Plenty Is No Plague: streptomyces symbiosis with crops.","volume":"22","author":"Rey","year":"2017","journal-title":"Trends Plant Sci."},{"key":"B44","doi-asserted-by":"crossref","DOI":"10.1007\/BF02980873","article-title":"Control of late blight in potato by full and reduced rates of oxadixyl mixtures.","volume":"21","author":"Samoucha","year":"1993","journal-title":"Phytoparasitica"},{"key":"B45","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1007\/s12298-016-0359-x","article-title":"Microbial secondary metabolites ameliorate growth, in planta contents and lignification in Withania somnifera (L.) Dunal.","volume":"22","author":"Singh","year":"2016","journal-title":"Physiol. Mol. Biol. Plants"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-19986-1","article-title":"Comprehensive prediction of secondary metabolite structure and biological activity from microbial genome sequences.","volume":"11","author":"Skinnider","year":"2020","journal-title":"Nat. Commun."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1359","DOI":"10.4014\/jmb.1203.02056","article-title":"Biocontrol of anthracnose in pepper using chitinase, \u03b2-1,3 glucanase, and 2-furancarboxaldehyde produced by Streptomyces cavourensis SY224.","volume":"22","author":"So Youn","year":"2012","journal-title":"J. Microbiol. Biotechnol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1007\/s00128-012-0765-x","article-title":"Comparison of greenhouse and field degradation behaviour of isoprocarb, hexaflumuron and difenoconazole in Perilla frutescens.","volume":"89","author":"Sun","year":"2012","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"B49","doi-asserted-by":"crossref","first-page":"1691","DOI":"10.1099\/mic.0.27758-0","article-title":"Secondary metabolites from endophytic Streptomyces aureofaciens CMUAc130 and their antifungal activity.","volume":"151","author":"Taechowisan","year":"2005","journal-title":"Microbiology"},{"key":"B50","doi-asserted-by":"publisher","first-page":"3002","DOI":"10.1016\/j.bbagen.2016.09.029","article-title":"Ebselen exerts antifungal activity by regulating glutathione (GSH) and reactive oxygen species (ROS) production in fungal cells.","volume":"1861","author":"Thangamani","year":"2017","journal-title":"Biochim. Biophys. Acta Gen. SUBJ."},{"key":"B51","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1038\/nchembio.2319","article-title":"A new genome-mining tool redefines the lasso peptide biosynthetic landscape.","volume":"13","author":"Tietz","year":"2017","journal-title":"Nat. Chem. Biol."},{"key":"B52","doi-asserted-by":"publisher","first-page":"2161","DOI":"10.1128\/AEM.68.5.2161-2171.2002","article-title":"Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum).","volume":"68","author":"Tokala Ranjeet","year":"2002","journal-title":"Appl. Environ. Microbiol."},{"key":"B53","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1016\/j.cell.2005.07.017","article-title":"Inhibition of bacterial RNA polymerase by Streptolydigin: stabilization of a straight-bridge-helix active-center conformation.","volume":"122","author":"Tuske","year":"2005","journal-title":"Cell"},{"key":"B54","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1002\/jobm.201000155","article-title":"Bio-control and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss.","volume":"51","author":"Verma","year":"2011","journal-title":"J. Basic Microbiol."},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.00942","article-title":"Streptomyces lydicus M01 regulates soil microbial community and alleviates foliar disease caused by Alternaria alternata on cucumbers.","volume":"11","author":"Wang","year":"2020","journal-title":"Front. Microbiol."},{"key":"B56","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1007\/s002030100345","article-title":"How many antibiotics are produced by the genus Streptomyces?","volume":"176","author":"Watve","year":"2001","journal-title":"Arch. Microbiol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"3119","DOI":"10.1128\/aem.61.8.3119-3128.1995","article-title":"Characterization of streptomyces lydicus WYEC108 as a potential biocontrol agent against fungal root and seed rots.","volume":"61","author":"Yuan","year":"1995","journal-title":"Appl. Environ. Microbiol."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.908879\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,31]],"date-time":"2022-05-31T03:59:36Z","timestamp":1653969576000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2022.908879\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,31]]},"references-count":57,"alternative-id":["10.3389\/fmicb.2022.908879"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2022.908879","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,31]]},"article-number":"908879"}}