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Volatile organic compounds profile synthesized and released by endophytes of tomato (Solanum lycopersici L.) and their antagonistic role

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Abstract

The endophytic microbiome uses mechanisms such as the secretion of diffusible antibiotic molecules, synthesis and release of volatile organic compounds, and/or toxins to protect plants. The aim of this research was to study the volatile organic compounds (VOCs) profile as well as the diffusible secondary metabolites produced and released by endophytic bacteria isolated from tomato plants that in in-vitro assays prevented growth of pathogenic fungi. Bacteria belonging to seven genera (Acinetobacter, Arthrobacter, Bacillus, Microbacterium, Pantoea, Pseudomonas, and Stenotrophomonas) were isolated from different tissues of tomato plants with and without symptoms of Gray leaf spot, a disease provoked by Stemphylium lycopersici. In vitro, antagonistic assays were performed and the effect of volatile and soluble compounds released by endophytic bacteria on the growth of pathogenic fungi was determined. The VOCs synthesized by the endophytes were extracted, identified and quantified. These isolates representatives of seven bacterial genera inhibited the growth of three fungal pathogens of tomato S. lycopersici, Alternaria alternata and Corynespora cassiicola, which was related to the synthesis of soluble compounds as well as VOCs. Endophytes synthesize and release different VOCs, probably due to the different type of interaction that each bacterium establishes with the fungus, presenting a range of fungal growth inhibition.

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References

  • Ab Rahman SFS, Singh E, Pieterse CM, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111

    Google Scholar 

  • Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR (2018) Bacterial quorum sensing and microbial community interactions. MBio 9(3):e02331-e2417

    CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen RA, Hamilton-Kemp TR, Hildebrand DF, McCracken CT Jr, Collins RW, Fleming PD (1994) Structure-antifungal activity relationships among volatile C6 and C9 aliphatic aldehydes, ketones, and alcohols. J Agric Food Chem 42(7):1563–1568

    CAS  Google Scholar 

  • Ando H, Hatanaka K, Ohata I, Yamashita-Kitaguchi Y, Kurata A, Kishimoto N (2012) Antifungal activities of volatile substances generated by yeast isolated from Iranian commercial cheese. Food Control 26(2):472–478

    CAS  Google Scholar 

  • Bader AN, Salerno GL, Covacevich F, Consolo VF (2020) Native Trichoderma harzianum strains from Argentina produce indole-3 acetic acid and phosphorus solubilization, promote growth and control wilt disease on tomato (Solanum lycopersicum L.). J King Saud Univ Sci 32(1):867–873

    Google Scholar 

  • Balzarini MG, Gonzalez L, Tablada M, Casanoves F, Di Rienzo JA, Robledo CW (2008) Infostat. Manual del usuario, Editorial Brujas, Córdoba, Argentina, p 336

    Google Scholar 

  • Baysal Ö, Lai D, Xu HH, Siragusa M, Çalışkan M, Carimi F, Teixeira da Silva JA, Tör M (2013) A proteomic approach provides new insights into the control of soil-borne plant pathogens by Bacillus species. PLoS One 8(1):e53182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chiron N, Michelot D (2005) Odeurs des champignons: chimie et rôle dans les interactions biotiques-une revue. Cryptogam Mycol 26(4):299–364

    Google Scholar 

  • Claeson AS, Sandström M, Sunesson AL (2007) Volatile organic compounds (VOCs) emitted from materials collected from buildings affected by microorganisms. J Environ Monit 9(3):240–245

    CAS  PubMed  Google Scholar 

  • Collinge DB, Jørgensen HJ, Latz M, Manzotti A, Ntana F, Rojas Tayo EC, Jensen B (2019) Searching for novel fungal biological control agents for plant disease control among endophytes. Endophytes Grow World 21:25–51

    Google Scholar 

  • De Boer W (2017) Upscaling of fungal–bacterial interactions: from the lab to the field. Curr Opin Microbiol 37:35–41

    PubMed  Google Scholar 

  • Dukare AS, Paul S, Nambi VE, Gupta RK, Singh R, Sharma K, Vishwakarma RK (2019) Exploitation of microbial antagonists for the control of postharvest diseases of fruits: a review. Crit Rev Food Sci Nutr 59(9):1498–1513

    CAS  PubMed  Google Scholar 

  • Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38(6):665–703

    CAS  PubMed  Google Scholar 

  • Elgaali H, Hamilton-Kemp TR, Newman MC, Collins RW, Yu K, Archbold DD (2002) Comparison of long-chain alcohols and other volatile compounds emitted from food-borne and related Gram positive and Gram negative bacteria. J Basic Microbiol 42(6):373–380

    CAS  PubMed  Google Scholar 

  • Etschmann M, Bluemke W, Sell D, Schrader J (2002) Biotechnological production of 2-phenylethanol. Appl Microbiol Biotechnol 59(1):1–8

    CAS  PubMed  Google Scholar 

  • Franco MEE, Troncozo MI, López SMY, Lucentini G, Medina R, Saparrat MCN, Ronco LB, Balatti PA (2017) A survey on tomato leaf grey spot in the two main production areas of Argentina led to the isolation of Stemphylium lycopersici representatives which were genetically diverse and differed in their virulence. Eur J Plant Pathol 149(4):983–1000

    Google Scholar 

  • Garbeva P, Hordijk C, Gerards S, de Boer W (2014) Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol Ecol 87:639–649. https://doi.org/10.1111/1574-6941.12252

    Article  CAS  PubMed  Google Scholar 

  • Hamilton-Kemp T, Newman M, Collins R, Elgaali H, Yu K, Archbold D (2005) Production of the long-chain alcohols octanol, decanol, and dodecanol by Escherichia coli. Curr Microbiol 51(2):82–86

    CAS  PubMed  Google Scholar 

  • Hunziker L, Bönisch D, Groenhagen U, Bailly A, Schulz S, Weisskopf L (2015) Pseudomonas strains naturally associated with potato plants produce volatiles with high potential for inhibition of Phytophthora infestans. Appl Environ Microbiol 81:821–830. https://doi.org/10.1128/AEM.02999-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingram LO, Buttke TM (1984) Effects of alcohols on microrganismos. Adv Microbiol Physiol Bethesda 25:256–300

    Google Scholar 

  • Javidnia K, Faghih-Mirzaei E, Miri R, Attarroshan M, Zomorodian K (2016) Biotransformation of acetoin to 2, 3-butanediol: Assessment of plant and microbial biocatalysts. Res Pharm Sci 11(4):349

    PubMed  PubMed Central  Google Scholar 

  • Kabelitz N, Santos PM, Heipieper HH (2003) Effect of aliphatic alcohols on growth and degree of saturation of membrane lipids in Acinetobacter calcoaceticus. FEMS Microbiol Lett 220:223–227

    CAS  PubMed  Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187(5):351–360

    CAS  PubMed  Google Scholar 

  • Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B (2009) Bacterial volatiles and their action potential. Appl Environ Microbiol 81:1001–1012. https://doi.org/10.1007/s00253-008-1760-3

    Article  CAS  Google Scholar 

  • Kakoti P, Gogoi P, Yadav A, Singh BP, Saikia R (2020) Foliar Fungal Diseases in Pulses: Review and Management. Management of Fungal Pathogens in Pulses. Springer, Cham, pp 131–142

    Google Scholar 

  • Kerdraon L, Laval V, Suffert F (2019) Microbiomes and pathogen survival in crop residues, an ecotone between plant and soil. Phytobiomes J 3(4):246–255

    Google Scholar 

  • Kim KS, Lee S, Ryu CM (2013) Interspecific bacterial sensing through airborne signals modulates locomotion and drug resistance. Nat Commun 4(1):1–12

    Google Scholar 

  • Köhl J, Kolnaar R, Ravensberg WJ (2019) Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci 10:845

    PubMed  PubMed Central  Google Scholar 

  • Kubo I, Fujita T, Kubo A, Fujita K (2003) Modes of antifungal action of alcohols against Saccharomyces cerevisiae. Biorg Med Chem 11:1117–1122

    CAS  Google Scholar 

  • Kubo I, Muroi H, Kubo A (1995) Structural functions of antimicrobial long-chain alcohols and phenols. Bioorg Med Chem 3(7):873–880

    CAS  PubMed  Google Scholar 

  • Le Cocq K, Gurr SJ, Hirsch PR, Mauchline TH (2017) Exploitation of endophytes for sustainable agricultural intensification. Mol Plant Pathol 18(3):469–473

    PubMed  Google Scholar 

  • Lecomte C, Alabouvette C, Edel-Hermann V, Robert F, Steinberg C (2016) Biological control of ornamental plant diseases caused by Fusarium oxysporum: a review. Biol Control 101:17–30

    Google Scholar 

  • Lemfack MC, Nickel J, Dunkel M, Preissner R, Piechulla B (2014) mVOC: a database of microbial volatiles. Nucleic Acids Res 42(D1):D744–D748

    CAS  PubMed  Google Scholar 

  • Li L, Wang Y, Li K, Su F, Ma C, Xu P (2014) Genome sequence of meso-2, 3-butanediol-producing strain Serratia marcescens ATCC 14041. Genome Announce. 2(3)

  • Li Q, Ning P, Zheng L, Huang J, Li G, Hsiang T (2010) Fumigant activity of volatiles of Streptomyces globisporus JK-1 against Penicillium italicum on Citrus microcarpa. Postharvest Biol Technol 58(2):157–165

    CAS  Google Scholar 

  • Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CM, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbial 8:2552

    Google Scholar 

  • Liu WW, Wei MU, Zhu BY, Du YC, Feng LIU (2008) Antagonistic activities of volatiles from four strains of Bacillus spp. and Paenibacillus spp against soil-borne plant pathogens. Agric Sci China 7(9):1104–1114

    CAS  Google Scholar 

  • López SMY, Pastorino GN, Fernández-González AJ, Franco MEE, Fernández-López M, Balatti PA (2020) The Endosphere bacteriome of diseased and healthy tomato plants. Microbiol, Arch. https://doi.org/10.1007/s00203-020-01987-9

    Book  Google Scholar 

  • López SMY, Pastorino GN, Franco MEE, Medina R, Lucentini CG, Saparrat MCN, Balatti PA (2018) Microbial endophytes that live within the seeds of two tomato hybrids cultivated in Argentina. Agronomy 8(8):136

    Google Scholar 

  • Lucchini JJ, Bonnaveiro N, Cremieux A, Le Goffic F (1993) Mechanism of bactericidal action of phenethyl alcohol in Escherichia coli. Curr Microbiol 27(5):295–300

    CAS  Google Scholar 

  • Ludwig-Müller J (2015) Plants and endophytes: equal partners in secondary metabolite production? Biotechnol Lett 37(7):1325–1334

    PubMed  Google Scholar 

  • Maruzzella JC, Chiaramonte JS, Garofalo MM (1961) Effects of vapors of aromatic chemicals on fungi. J Pharm Sci 50(8):665–668

    CAS  Google Scholar 

  • Medina R, Franco ME, Lucentini CG, Rosso JA, Saparrat MC, Bartel LC, Balatti PA (2019) Secondary metabolites synthesized by Stemphylium lycopersici and Fulvia fulva, necrotrophic and biotrophic fungi pathogen of tomato plants. Curr Plant Biol 20:100122

    Google Scholar 

  • Molina-Santiago C, Daddaoua A, Fillet S, Duque E, Ramos JL (2014) Interspecies signalling: P seudomonas putida efflux pump TtgGHI is activated by indole to increase antibiotic resistance. Environ Microbiol 16(5):1267–1281

    CAS  PubMed  Google Scholar 

  • Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26(2–3):73–83

    Google Scholar 

  • Morita T, Tanaka I, Ryuda N, Ikari M, Ueno D, Someya T (2019) Antifungal spectrum characterization and identification of strong volatile organic compounds produced by Bacillus pumilus TM-R. Heliyon. https://doi.org/10.1016/j.heliyon.2019.e01817

    Article  PubMed  PubMed Central  Google Scholar 

  • Nair DN, Padmavathy S (2014) Impact of endophytic microorganisms on plants, environment and humans. Sci World J. https://doi.org/10.1155/2014/250693

    Article  Google Scholar 

  • Naznin HA, Kiyohara D, Kimura M, Miyazawa M, Shimizu M, Hyakumachi M (2014) Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS ONE 9:e86882. https://doi.org/10.1371/journal.pone.0086882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piechulla B, Degenhardt J (2014) The emerging importance of microbial volatile organic compounds. Plant Cell Environ 37(4):811–812

    CAS  PubMed  Google Scholar 

  • Popova AA, Koksharova OA, Lipasova VA, Zaitseva JV, Katkova-Zhukotskaya OA, Eremina SI et al (2014) Inhibitory and toxic effects of volatiles emitted by strains of Pseudomonas and Serratia on growth and survival of selected microorganisms, Caenorhabditis elegans, and Drosophila melanogaster. Biomed Res Int. https://doi.org/10.1155/2014/125704

    Article  PubMed  PubMed Central  Google Scholar 

  • Prakash B, Singh P, Goni R, Raina AKP, Dubey NK (2015) Efficacy of Angelica archangelica essential oil, phenyl ethyl alcohol and α-terpineol against isolated molds from walnut and their antiaflatoxigenic and antioxidant activity. J Food Sci Technol 52(4):2220–2228

    CAS  PubMed  Google Scholar 

  • Raza W, Yuan J, Ling N, Huang Q, Shen Q (2015) Production of volatile organic compounds by an antagonistic strain Paenibacillus polymyxa WR-2 in the presence of root exudates and organic fertilizer and their antifungal activity against Fusarium oxysporum f. sp. niveum. Biol Control 80:89–95

    CAS  Google Scholar 

  • Rodríguez-Ortega WM, Martínez V, Nieves M, Simón I, Lidón V, Fernandez-Zapata JC, Martinez-Nicolas JJ, Cámara-Zapata JM, García-Sánchez F (2019) Agricultural and physiological responses of tomato plants grown in different soilless culture systems with saline water under greenhouse conditions. Sci Rep 9(1):1–13

    Google Scholar 

  • Romoli R, Papaleo MC, De Pascale D, Tutino ML, Michaud L, LoGiudice A, Fani R, Bartolucci G (2014) GC–MS volatolomic approach to study the antimicrobial activity of the antarctic bacterium Pseudoalteromonas sp. TB41. Metabolomics 10(1):42–51

    CAS  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19(8):827–837

    CAS  PubMed  Google Scholar 

  • Rudrappa T, Biedrzycki ML, Kunjeti SG, Donofrio NM, Czymmek KJ, Paré PW et al (2010) The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun Integr Biol 3:130–138. https://doi.org/10.4161/cib.3.2.10584

    Article  PubMed  PubMed Central  Google Scholar 

  • Schmidt R, Cordovez V, De Boer W, Raaijmakers J, Garbeva P (2015) Volatile affairs in microbial interactions. ISME J 9(11):2329–2335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Snelders NC, Kettles GJ, Rudd JJ, Thomma BP (2018) Plant pathogen effector proteins as manipulators of host microbiomes? Mol Plant Pathol 19(2):257

    PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Fukuda S, Kikuzaki H, Nakatani N (2000) Antibacterial activity of aliphatic long chain compounds against upper airway respiratory tract bacteria. ITE Lett. Batteries. New Technol Med 1:C35–C38

    Google Scholar 

  • Thomashow LS, Kwak YS, Weller DM (2019) Root-associated microbes in sustainable agriculture: models, metabolites and mechanisms. Pest Manage Sci 75(9):2360–2367

    CAS  Google Scholar 

  • Tilocca B, Cao A, Migheli Q (2020) Scent of a Killer: microbial volatilome and its role in the biological control of plant pathogens. Front Microbiol. https://doi.org/10.3389/fmicb.2020.00041

    Article  PubMed  PubMed Central  Google Scholar 

  • Tyc O, Song C, Dickschat JS, Vos M, Garbeva P (2017) The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends Microbiol 25(4):280–292

    CAS  PubMed  Google Scholar 

  • Urbanek A, Szadziewski R, Stepnowski P, Boros-Majewska J, Gabriel I, Dawgul M et al (2012) Composition and antimicrobial activity of fatty acids detected in the hygroscopic secretion collected from the secretory setae of larvae of the biting midge Forcipomyia nigra (Diptera: Ceratopogonidae). J Insect Physiol 58(9):1265–1276

    CAS  PubMed  Google Scholar 

  • Wang C, Wang Z, Qiao X, Li Z, Li F, Chen M et al (2013) Antifungal activity of volatile organic compounds from Streptomyces alboflavus TD-1. FEMS Microbiol Lett 341:45–51. https://doi.org/10.1111/1574-6968.12088

    Article  CAS  PubMed  Google Scholar 

  • Weisskopf L (2013) The potential of bacterial volatiles for crop protection against phytophathogenic fungi Microb Pathog Strategies for combating them. Sci Technol Educ 2:1352–1363

    Google Scholar 

  • Wheatley R, Hackett C, Bruce A, Kundzewicz A (1997) Effect of substrate composition on production of volatile organic compounds from Trichoderma spp inhibitory to wood decay fungi. Int Biodeterior Biodegrad 39(2–3):199–205

    CAS  Google Scholar 

  • Wu Y, Zhou J, Li C, Ma Y (2019) Antifungal and plant growth promotion activity of volatile organic compounds produced by Bacillus amyloliquefaciens. MicrobiologyOpen 8(8):e00813

    PubMed  PubMed Central  Google Scholar 

  • Yuan J, Raza W, Shen Q, Huang Q (2012) Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. cubense. Appl Environ Microbiol 78(16):5942–5944

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We wish to thank Dr. Sergio Mijailovsky from Institute of Investigaciones Bioquímicas de La Plata (CONICET-UNLP, La Plata, Argentina) for his help in performing the extraction, identification and quantification of VOCs and their analysis.

Funding

This research was partially supported by the Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CICBA), Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) of the Ministerio de Ciencia, Tecnología e Innovación Productiva through the projects PICT-2016–0794 Jóvenes Investigadores (Silvina López) and the CICBA through the Subsidio 2017 (Pedro Balatti). http://www.agencia.mincyt.gob.ar; https://www.gba.gob.ar/cic.

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Authors and Affiliations

  1. Centro de Investigaciones en Fitopatología (CIDEFI), La Plata, Argentina

    Silvina M. Y. López & Pedro Alberto Balatti

  2. Comisión de Investigaciones Científicas de La Provincia de Buenos Aires (CICBA), La Plata, Argentina

    Silvina M. Y. López & Pedro Alberto Balatti

  3. Cátedra de Microbiología Agrícola, Universidad Nacional de La Plata (UNLP), Calle 60 y 119, La Plata, C. P. 1900, Buenos Aires, Argentina

    Graciela Noemi Pastorino & Pedro Alberto Balatti

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  1. Silvina M. Y. López
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  2. Graciela Noemi Pastorino
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  3. Pedro Alberto Balatti
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Contributions

The contributions of the authors in carrying out this work are detailed below: conceptualization, López SMY and Balatti PA; methodology, López SMY and Pastorino GN; software and validation, López SMY and Balatti PA; formal analysis, López SMY and Pastorino GN; research, López SMY; writing—preparation of the original draft, López SMY and Balatti PA; writing—review and editing, López SMY and Balatti PA; Project Management and Fund Acquisition, López SMY and Balatti PA.

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Correspondence to Silvina M. Y. López.

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López, S.M.Y., Pastorino, G.N. & Balatti, P.A. Volatile organic compounds profile synthesized and released by endophytes of tomato (Solanum lycopersici L.) and their antagonistic role. Arch Microbiol 203, 1383–1397 (2021). https://doi.org/10.1007/s00203-020-02136-y

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