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Study of in vitro interaction between Fusarium verticillioides and Streptomyces sp. using metabolomics

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Abstract

The Streptomyces sp. strain AV05 isolated from an organic amendment was found to impact both growth and fumonisin production of Fusarium verticillioides during in vitro direct confrontation. In order to investigate the interactions between the Streptomyces sp. strain AV05 and F. verticillioides, a metabolomic approach was used. The study of the endometabolomes of the microorganisms was carried out in two different conditions: the microorganisms were cultivated alone or in confrontation. The aim of this study was to examine the modifications of the endometabolome of F. verticillioides in confrontation with the Streptomyces strain. The metabolites involved in these modifications were identified using 2D NMR. Many metabolites were found to be overproduced in confrontation assays with the Streptomyces strain, notably 16 proteinogenic amino acids, inosine, and uridine. This suggested that fungal metabolic pathways such as protein synthesis have been affected due to interaction. Thus, metabolomic studies, as well as proteomics or transcriptomics, are useful for deciphering the mechanisms of interactions between biological control agents and mycotoxigenic fungi. This comprehension is one of the key elements of the improvement of the selection and use of antagonistic agents.

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References

  • Barrans A, Collet X, Barbaras R, Jaspard B, Manent J, Vieu C, Chap H, Perret B (1994) Hepatic lipase induces the formation of pre-beta 1 high density lipoprotein (HDL) from triacylglycerol-rich HDL2. A study comparing liver perfusion to in vitro incubation with lipases. J Biol Chem 269:11572–11577

    CAS  PubMed  Google Scholar 

  • Bohni N, Hofstetter V, Gindro K, Buyck B, Schumpp O, Bertrand S, Monod M, Wolfender JL (2016) Production of fusaric acid by Fusarium spp. in pure culture and in solid medium co-cultures. Molecules 21:370

    PubMed  PubMed Central  Google Scholar 

  • Bojja RS, Cerny RL, Proctor RH, Du L (2004) Determining the biosynthetic sequence in the early steps of the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J Agric Food Chem 52:2855–2860

    CAS  PubMed  Google Scholar 

  • Chopra A (1984) Lipid metabolism in fungi. CRC Crit Rev Microbiol 11:209–271

    CAS  Google Scholar 

  • Chu FS, Li GY (1994) Simultaneous occurrence of fumonisin B1 and other mycotoxins in moldy corn collected from the People’s Republic of China in regions with high incidences of esophageal cancer. Appl Environ Microbiol 60:47–852

    Google Scholar 

  • Davies F, Williams S (1970) Studies on the ecology of actinomycetes in soil: I. The occurrence and distribution of actinomycetes in a pine forest soil. Soil Biol Biochem 2:227–238

    Google Scholar 

  • Dombou CL, Salove MKH, Crawford DL, Beaulieu C (2001) Actinomycetes, promising tools to control plant diseases and to promote plant growth. Phytoprotection 82:85–102

    Google Scholar 

  • Eshelli M, Harvey L, Edrada-Ebel R, McNeil B (2015) Metabolomics of the bio-degradation process of aflatoxin B1 by actinomycetes at an initial pH of 6. 0. Toxins 7:439–456

    CAS  PubMed  PubMed Central  Google Scholar 

  • Evangelista-Martínez Z (2014) Isolation and characterization of soil Streptomyces species as potential biological control agents against fungal plant pathogens. World J Microbiol Biotechnol 30:1639–1647

    PubMed  Google Scholar 

  • Fleck CB, Schöbel F, Brock M (2011) Nutrient acquisition by pathogenic fungi: nutrient availability, pathway regulation, and differences in substrate utilization. Int J Med Microbiol 301:400–407

    CAS  PubMed  Google Scholar 

  • Frändberg E, Petersson C, Lundgren LN, Schnürer J (2000) Streptomyces halstedii K122 produces the antifungal compounds bafilomycin B1 and C1. Can J Microbiol 46:753–758

    PubMed  Google Scholar 

  • Frisvad JC (2014) Taxonomy, chemodiversity, and chemoconsistency of Aspergillus, Penicillium, and Talaromyces species. Front Microbiol 5:773

    PubMed  Google Scholar 

  • Giannitti F, Diab SS, Pacin AM, Barrandeguy M, Larrere C, Ortega J, Uzal FA (2011) Equine leukoencephalomalacia (ELEM) due to fumonisins B1 and B2 in Argentina. Pesqui Vet Bras 31:407–412

    Google Scholar 

  • Guo Y, Zheng W, Rong X, Huang Y (2008) A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 58:149–159

    CAS  PubMed  Google Scholar 

  • Harkai P, Szabó I, Cserháti M, Krifaton C, Risa A, Radó J, Balázs A, Berta K, Kriszt B (2016) Biodegradation of aflatoxin-B1 and zearalenone by Streptomyces sp. collection. Int Biodeterior Biodegradation 108:48–56

    CAS  Google Scholar 

  • Heinl S, Hartinger D, Thamhesl M, Vekiru E, Krska R, Schatzmayr G, Moll WD, Grabherr R (2010) Degradation of fumonisin B1 by the consecutive action of two bacterial enzymes. J Biotechnol 145:120–129

    CAS  PubMed  Google Scholar 

  • Huffman J, Gerber R, Du L (2010) Recent advancements in the biosynthetic mechanisms for polyketide-derived mycotoxins. Biopolymers 93:764–776

    CAS  PubMed  PubMed Central  Google Scholar 

  • Idnurm A, Howlett BJ (2002) Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola (Brassica napus). Eukaryot Cell 1:719–724

    CAS  PubMed  PubMed Central  Google Scholar 

  • Isaacson C (2005) The change of the staple diet of black South Africans from sorghum to maize (corn) is the cause of the epidemic of squamous carcinoma of the oesophagus. Med Hypotheses 64:658–660

    CAS  PubMed  Google Scholar 

  • Joo GJ (2005) Production of an anti-fungal substance for biological control of Phytophthora capsici causing phytophthora blight in red-peppers by Streptomyces halstedii. Biotechnol Lett 27:201–205

    CAS  PubMed  Google Scholar 

  • Khieu TN, Liu MJ, Nimaichand S, Quach NT, Chu-Ky S, Phi QT, Vu TT, Nguyen TD, Xiong Z, Prabhu DM (2015) Characterization and evaluation of antimicrobial and cytotoxic effects of Streptomyces sp. HUST012 isolated from medicinal plant Dracaena cochinchinensis Lour. Front Microbiol 6:574

    PubMed  PubMed Central  Google Scholar 

  • Kunova A, Bonaldi M, Saracchi M, Pizzatti C, Chen X, Cortesi P (2016) Selection of Streptomyces against soil borne fungal pathogens by a standardized dual culture assay and evaluation of their effects on seed germination and plant growth. BMC Microbiol 16:272–283

    PubMed  PubMed Central  Google Scholar 

  • Lee EJ, Hwang KY, Lee HS, Chung N (2011) Characterization of a new Streptomyces sp. A1022 as a potential biocontrol agent. J Korean Soc Appl Biol Chem 54:488–493

    CAS  Google Scholar 

  • Lorenz MC, Fink GR (2001) The glyoxylate cycle is required for fungal virulence. Nature 412:83–86

    CAS  PubMed  Google Scholar 

  • Menon A, Eppinger M, Mayor S, Schwarz R (1993) Phosphatidylethanolamine is the donor of the terminal phosphoethanolamine group in trypanosome glycosylphosphatidylinositols. EMBO J 12:1907–1914

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minuto A, Spadaro D, Garibaldi A, Gullino ML (2006) Control of soilborne pathogens of tomato using a commercial formulation of Streptomyces griseoviridis and solarization. Crop Prot 25:468–475

    Google Scholar 

  • Nguyen PA, Strub C, Fontana A, Schorr-Galindo S (2017) Crop molds and mycotoxins: alternative management using biocontrol. Biol Control 104:10–27

    Google Scholar 

  • Nguyen PA, Strub C, Durand N, Alter P, Fontana A, Schorr-Galindo S (2018) Biocontrol of Fusarium verticillioides using organic amendments and their actinomycete isolates. Biol Control 118:55–66

    CAS  Google Scholar 

  • Niderkorn V, Morgavi D, Aboab B, Lemaire M, Boudra H (2009) Cell wall component and mycotoxin moieties involved in the binding of fumonisin B1 and B2 by lactic acid bacteria. J Appl Microbiol 106:977–985

    CAS  PubMed  Google Scholar 

  • Ola AR, Thomy D, Lai D, Brötz-Oesterhelt H, Proksch P (2013) Inducing secondary metabolite production by the endophytic fungus Fusarium tricinctum through coculture with Bacillus subtilis. J Nat Prod 76:2094–2099

    CAS  PubMed  Google Scholar 

  • Oskay M (2009) Antifungal and antibacterial compounds from Streptomyces strains. Afr J Biotechnol 8:3007–3017

    CAS  Google Scholar 

  • Pitt J (2000) Toxigenic fungi and mycotoxins. Br Med Bull 56:184–192

    CAS  PubMed  Google Scholar 

  • Prasad R, Ghannoum MA (1996) Lipids of pathogenic fungi. CRC press, New York

    Google Scholar 

  • Pugliese M, Gullino M, Garibaldi A (2009) Efficacy of microorganisms selected from compost to control soil-borne pathogens. Commun Agric Appl Biol Sci 75:665–669

    Google Scholar 

  • Rateb ME, Hallyburton I, Houssen WE, Bull AT, Goodfellow M, Santhanam R, Jaspars M, Ebel R (2013) Induction of diverse secondary metabolites in Aspergillus fumigatus by microbial co-culture. RSC Adv 3:4444–14450

    Google Scholar 

  • Rheeder JP, Marasas WF, Vismer HF (2002) Production of fumonisin analogs by Fusarium species. Appl Environ Microbiol 68:2101–2105

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rittenour WR, Harris SD (2013) Glycosylphosphatidylinositol-anchored proteins in Fusarium graminearum: inventory, variability, and virulence. PLoS One 8:e81603

    PubMed  PubMed Central  Google Scholar 

  • Samsudin NIP, Magan N (2016) Efficacy of potential biocontrol agents for control of Fusarium verticillioides and fumonisin B1 under different environmental conditions. World Mycotoxin J 9:205–213

    CAS  Google Scholar 

  • Sheridan KJ, Dolan SK, Doyle S (2014) Endogenous cross-talk of fungal metabolites. Front Microbiol 5:732

    PubMed  Google Scholar 

  • Soltanzadeh M, Soltani Nejad M, Shahidi Bonjar GH (2016) Application of soil-borne actinomycetes for biological control against Fusarium wilt of chickpea (Cicer arietinum) caused by Fusarium solani fsp pisi. J Phytopathol 164:967–978

    CAS  Google Scholar 

  • Suárez-Estrella F, Arcos-Nievas MA, López MJ, Vargas-García MC, Moreno J (2013) Biological control of plant pathogens by microorganisms isolated from agro-industrial composts. Biol Control 67:509–515

    Google Scholar 

  • Tanaka Y, Omura S (1993) Agroactive compounds of microbial origin. Annu Rev Microbiol 47:57–87

    CAS  PubMed  Google Scholar 

  • Wang ZY, Thornton CR, Kershaw MJ, Debao L, Talbot NJ (2003) The glyoxylate cycle is required for temporal regulation of virulence by the plant pathogenic fungus Magnaporthe grisea. Mol Microbiol 47:1601–1612

    CAS  PubMed  Google Scholar 

  • Wu C, Choi YH, van Wezel GP (2016) Metabolic profiling as a tool for prioritizing antimicrobial compounds. J Ind Microbiol Biotechnol 43:299–312

    CAS  PubMed  Google Scholar 

  • Yoshinari T, Akiyama T, Nakamura K, Kondo T, Takahashi Y, Muraoka Y, Nonomura Y, Nagasawa H, Sakuda S (2007) Dioctatin A is a strong inhibitor of aflatoxin production by Aspergillus parasiticus. Microbiology 153:2774–2780

    CAS  PubMed  Google Scholar 

  • Yoshizawa T, Yamashita A, Luo Y (1994) Fumonisin occurrence in corn from high-and low-risk areas for human esophageal cancer in China. Appl Environ Microbiol 60:1626–1629

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Rao R (2010) Beyond ergosterol: linking pH to antifungal mechanisms. Virulence 1:551–554

    PubMed  Google Scholar 

  • Zuck KM, Shipley S, Newman DJ (2011) Induced production of N-formyl alkaloids from Aspergillus fumigatus by co-culture with Streptomyces peucetius. J Nat Prod 74:1653–1657

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Our appreciations are sent to the platform PFEM (Plateforme d’Exploration du Métabolisme-Clermont-Ferrand, France) as well as the platform MétaToul (Plateforme de Métabolomique et Fluxomique de Toulouse-Toulouse, France) for supporting us in the metabolomic techniques.

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Correspondence to Caroline Strub.

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Nguyen, PA., Strub, C., Lagrée, M. et al. Study of in vitro interaction between Fusarium verticillioides and Streptomyces sp. using metabolomics. Folia Microbiol 65, 303–314 (2020). https://doi.org/10.1007/s12223-019-00725-z

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