Enhancing the yield of Xenocoumacin 1 in Xenorhabdus nematophila YL001 by optimizing the fermentation process.

Xenorhabdus nematophila Biopesticide Fermentation optimization Response surface methodology Xenocoumacin 1 (Xcn1)

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
12 06 2024
Historique:
received: 10 01 2024
accepted: 03 06 2024
medline: 13 6 2024
pubmed: 13 6 2024
entrez: 12 6 2024
Statut: epublish

Résumé

Xenocoumacin 1 (Xcn 1), antibiotic discovered from secondary metabolites of Xenorhabdus nematophila, had the potential to develop into a new pesticide due to its excellent activity against bacteria, oomycetes and fungi. However, the current low yield of Xcn1 limits its development and utilization. To improve the yield of Xcn1, response surface methodology was used to determine the optimal composition of fermentation medium and one factor at a time approach was utilized to optimize the fermentation process. The optimal medium composed of in g/L: proteose peptone 20.8; maltose 12.74; K

Identifiants

pubmed: 38866882
doi: 10.1038/s41598-024-63794-2
pii: 10.1038/s41598-024-63794-2
doi:

Substances chimiques

Culture Media 0
xenocoumacin 1 105688-01-5
Anti-Bacterial Agents 0
Benzopyrans 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

13506

Subventions

Organisme : National Natural Science Foundation of China
ID : 32072474

Informations de copyright

© 2024. The Author(s).

Références

Adeolu, M., Alnajar, S., Naushad, S. & Gupta, R. S. Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int. J. Syst. Evol. Micr. 66, 5575–5599 (2016).
doi: 10.1099/ijsem.0.001485
Guo, S. et al. Regulation of antimicrobial activity and xenocoumacins biosynthesis by pH in Xenorhabdus nematophila. Microb. Cell Fact. 16, 203 (2017).
doi: 10.1186/s12934-017-0813-7 pubmed: 29141647 pmcid: 5688692
Wang, Y. & Zhang, X. Influence of agitation and aeration on growth and antibiotic production by Xenorhabdus nematophila. World J. Microb. Biot. 23, 221–227 (2007).
doi: 10.1007/s11274-006-9217-2
Zhang, S. et al. Nematophin, an antimicrobial dipeptide compound from Xenorhabdus nematophila YL001 as a potent biopesticide for Rhizoctonia solani control. Front. Microbiol. 10, e01765 (2019).
Pantel, L. et al. Odilorhabdins, antibacterial agents that cause miscoding by binding at a new ribosomal site. Mol. Cell 70, 83–94 (2018).
doi: 10.1016/j.molcel.2018.03.001 pubmed: 29625040
Brachmann, A. O. et al. Reciprocal cross talk between fatty acid and antibiotic biosynthesis in a nematode symbiont. Angew. Chem. Int. Ed. Engl. 51, 12086–12089 (2012).
doi: 10.1002/anie.201205384 pubmed: 23097192
McInerney, B. V. et al. Biologically active metabolites from Xenorhabdus spp., Part 2. Benzopyran-1-one derivatives with gastroprotective activity. J. Nat. Prod. 54, 785–795 (1991).
doi: 10.1021/np50075a006 pubmed: 1955881
Reimer, D. et al. Xenortide biosynthesis by entomopathogenic Xenorhabdus nematophila. J. Nat. Prod. 77, 1976–1980 (2014).
doi: 10.1021/np500390b pubmed: 25080196
Reimer, D., Luxenburger, E., Brachmann, A. O. & Bode, H. B. A new type of pyrrolidine biosynthesis is involved in the late steps of xenocoumacin production in Xenorhabdus nematophila. ChemBioChem 10, 1997–2001 (2009).
doi: 10.1002/cbic.200900187 pubmed: 19598185
Masschelein, J., Jenner, M. & Challis, G. L. Antibiotics from Gram-negative bacteria: A comprehensive overview and selected biosynthetic highlights. Nat. Prod. Rep. 34, 712–783 (2017).
doi: 10.1039/C7NP00010C pubmed: 28650032
Yang, X. et al. Antifungal activity of xenocoumacin 1 from Xenorhabdus nematophilus var. pekingensis against Phytophthora infestans. World J. Microb. Biot. 27, 523–528 (2011).
doi: 10.1007/s11274-010-0485-5
Incedayi, G. et al. Relative potency of a novel acaricidal compound from Xenorhabdus, a bacterial genus mutualistically associated with entomopathogenic nematodes. Sci. Rep. 11, 11253 (2021).
doi: 10.1038/s41598-021-90726-1 pubmed: 34045620 pmcid: 8159955
Wei, J. et al. Acaricidal effect of the antimicrobial metabolite xenocoumacin 1 on spider mite control. J. Integr. Agr. 23, 948–959 (2024).
doi: 10.1016/j.jia.2023.06.008
Zumbrunn, C. et al. Synthesis and structure-activity relationship of xenocoumacin 1 and analogues as inhibitors of ribosomal protein synthesis. ChemMedChem 16, 891–897 (2021).
doi: 10.1002/cmdc.202000793 pubmed: 33236408
Chen, W. et al. Promiscuous enzymatic activity-aided multiple-pathway network design for metabolic flux rearrangement in hydroxytyrosol biosynthesis. Nat. Commun. 10, 960 (2019).
doi: 10.1038/s41467-019-08781-2 pubmed: 30814511 pmcid: 6393456
Weber, T. et al. Metabolic engineering of antibiotic factories: new tools for antibiotic production in actinomycetes. Trends Biotechnol. 33, 15–26 (2015).
doi: 10.1016/j.tibtech.2014.10.009 pubmed: 25497361
Jubelin, G. et al. FliZ is a global regulatory protein affecting the expression of flagellar and virulence genes in individual Xenorhabdus nematophila bacterial cells. Plos Genet. 9, e1003915 (2013).
doi: 10.1371/journal.pgen.1003915 pubmed: 24204316 pmcid: 3814329
Neubacher, N. et al. Symbiosis, virulence and natural-product biosynthesis in entomopathogenic bacteria are regulated by a small RNA. Nat. Microbiol. 5, 1481–1489 (2020).
doi: 10.1038/s41564-020-00797-5 pubmed: 33139881 pmcid: 7610847
Engel, Y. et al. The global regulators Lrp, LeuO, and HexA control secondary metabolism in entomopathogenic bacteria. Front. Microbiol. 8, e209 (2017).
doi: 10.3389/fmicb.2017.00209
Zhang, S. et al. CpxR negatively regulates the production of Xenocoumacin 1, a dihydroisocoumarin derivative produced by Xenorhabdus nematophila. MicrobiologyOpen 8, e00674 (2019).
doi: 10.1002/mbo3.674 pubmed: 29888873
Park, D. et al. Genetic analysis of xenocoumacin antibiotic production in the mutualistic bacterium Xenorhabdus nematophila. Mol. Microbiol. 73, 938–949 (2009).
doi: 10.1111/j.1365-2958.2009.06817.x pubmed: 19682255
Dong, Y. et al. Improving the yield of Xenocoumacin 1 enabled by in situ product removal. ACS Omega 5, 20391–20398 (2020).
doi: 10.1021/acsomega.0c02357 pubmed: 32832792 pmcid: 7439382
Qin, Y. et al. Improving the yield of Xenocoumacin 1 by P
Qin, Y. et al. Enhancing the production of Xenocoumacin 1 in Xenorhabdus nematophila CB6 by a combinatorial engineering strategy. J. Agr. Food. Chem. 71, 8959–8968 (2023).
doi: 10.1021/acs.jafc.3c01793
Matrawy, A. A., Khalil, A. I., Marey, H. S. & Embaby, A. M. Biovalorization of the raw agro-industrial waste rice husk through directed production of xylanase by Thermomyces lanuginosus strain A3–1 DSM 105773: a statistical sequential model. Biomass Conv. Bioref. 11, 2177–2189 (2021).
doi: 10.1007/s13399-020-00824-9
Matrawy, A. A., Marey, H. S. & Embaby, A. M. The agro-industrial byproduct wheat bran as an inducer for alkaline protease (ALK-PR23) production by pschyrotolerant Lysinibacillus sphaericus strain AA6 EMCCN3080. Waste. Biomass Valor. 15, 1943–1958 (2024).
doi: 10.1007/s12649-023-02283-5
Embaby, A. M. et al. A novel non-cumbersome approach towards biosynthesis of pectic-oligosaccharides by non-aflatoxigenic Aspergillus sp. section Flavi strain EGY1 DSM 101520 through citrus pectin fermentation. PLoS One 11, e0167981 (2016).
doi: 10.1371/journal.pone.0167981 pubmed: 27992459 pmcid: 5167267
Anan, A. et al. Statistically optimized ceftriaxone sodium biotransformation through Achromobacter xylosoxidans strain Cef6: an unusual insight for bioremediation. J. Basic Microbiol. 58, 120–130 (2018).
doi: 10.1002/jobm.201700497 pubmed: 29141102
Sa-uth, C., Rattanasena, P., Chandrapatya, A. & Bussaman, P. Modification of medium composition for enhancing the production of antifungal activity from Xenorhabdus stockiae PB09 by using response surface methodology. Int. J. Microbiol. 2018, 3965851 (2018).
doi: 10.1155/2018/3965851 pubmed: 30008748 pmcid: 6020484
Wang, Y., Li, Y., Zhang, Q. & Zhang, X. Enhanced antibiotic activity of Xenorhabdus nematophila by medium optimization. Biores. Technol. 99, 1708–1715 (2008).
doi: 10.1016/j.biortech.2007.03.053
Wang, Y., Fang, X., Cheng, Y. & Zhang, X. Manipulation of pH shift to enhance the growth and antibiotic activity of Xenorhabdus nematophila. J. Biomed. Biotechnol. 2011, e672369 (2011).
doi: 10.1155/2011/672369
Wang, Y. H., Feng, J. T., Zhang, Q. & Zhang, X. Optimization of fermentation condition for antibiotic production by Xenorhabdus nematophila with response surface methodology. J. Appl. Microbiol. 104, 735–744 (2008).
doi: 10.1111/j.1365-2672.2007.03599.x pubmed: 17953686
Hassan, A. et al. Optimization of enhanced microbial production of zinc bacitracin by submerged fermentation technology. J. Basic. Microb. 60, 585–599 (2020).
doi: 10.1002/jobm.201900694
Teijaro, C. N., Adhikari, A. & Shen, B. Challenges and opportunities for natural product discovery, production, and engineering in native producers versus heterologous hosts. J. Ind. Microbiol. Biot. 46, 433–444 (2019).
doi: 10.1007/s10295-018-2094-5
Beltrametti, F. et al. Valine influences production and complex composition of glycopeptide antibiotic A40926 in fermentations of Nonomuraea sp. ATCC 39727. J. Antibiot. (Tokyo) 57, 37–44 (2004).
doi: 10.7164/antibiotics.57.37 pubmed: 15032484
Ng, I. S. et al. Daptomycin antibiotic production processes in fed-batch fermentation by Streptomyces roseosporus NRRL11379 with precursor effect and medium optimization. Bioprocess Biosyst. Eng. 37, 415–423 (2014).
doi: 10.1007/s00449-013-1007-2 pubmed: 23828246
Reimer, D. et al. A natural prodrug activation mechanism in nonribosomal peptide synthesis. Nat. Chem. Biol. 7, 888–890 (2011).
doi: 10.1038/nchembio.688 pubmed: 21926994
Fang, X. et al. Molecular identification and cultivation characteristics of entomopathogenic bacteria. J. NWAFU. (Nat. Sci. Ed.) 36, 199–204 (2008).
Reimer, D. & Bode, H. B. A natural prodrug activation mechanism in the biosynthesis of nonribosomal peptides. Nat. Prod. Rep. 31, 154–159 (2014).
doi: 10.1039/C3NP70081J pubmed: 24356302

Auteurs

Yunfei Han (Y)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
Shaanxi Research Center of Biopesticide Engineering & Technology, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.

Shujing Zhang (S)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests, Ministry of Education, School of Tropical Agriculture and Forestry (School of Agricultural and Rural Affairs, School of Rural Revitalization), Hainan University, 58 People's Avenue, Haikou, 570228, Hainan, China.

Yang Wang (Y)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
Shaanxi Research Center of Biopesticide Engineering & Technology, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.

Jiangtao Gao (J)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
Shaanxi Research Center of Biopesticide Engineering & Technology, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.

Jinhua Han (J)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
Shaanxi Research Center of Biopesticide Engineering & Technology, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.

Zhiqiang Yan (Z)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
Shaanxi Research Center of Biopesticide Engineering & Technology, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.

Yongquan Ta (Y)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.
Shaanxi Research Center of Biopesticide Engineering & Technology, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China.

Yonghong Wang (Y)

Key Laboratory of Plant Protection Resources and Pest Management, Ministry of Education, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China. yhwang@nwafu.edu.cn.
Shaanxi Research Center of Biopesticide Engineering & Technology, College of Plant Protection, Northwest A&F University, 22 Xinong Road, Yangling, 712100, Shaanxi, China. yhwang@nwafu.edu.cn.

Articles similaires

Vancomycin-associated DRESS demonstrates delay in AST abnormalities.

Ahmed Hussein, Kateri L Schoettinger, Jourdan Hydol-Smith et al.
1.00
Humans Drug Hypersensitivity Syndrome Vancomycin Female Male
Humans Arthroplasty, Replacement, Elbow Prosthesis-Related Infections Debridement Anti-Bacterial Agents
Aspergillus Hydrogen-Ion Concentration Coculture Techniques Secondary Metabolism Streptomyces rimosus
Vancomycin Polyesters Anti-Bacterial Agents Models, Theoretical Drug Liberation

Classifications MeSH