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Antagonistic bacteria of composted agro-industrial residues exhibit antibiosis against soil-borne fungal plant pathogens and protection of tomato plants from Fusarium oxysporum f.sp. radicis-lycopersici

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Abstract

Rhizospheric and root-associated/endophytic (RAE) bacteria were isolated from tomato plants grown in three suppressive compost-based plant growth media derived from the olive mill, winery and Agaricus bisporus production agro-industries. Forty-four (35 rhizospheric and 9 RAE) out of 329 bacterial strains showed in vitro antagonistic activity against at least one of the soil-borne fungal pathogens, Fusarium oxysporum f.sp. radicis-lycopersici (FORL), F. oxysporum f.sp. raphani, Phytophthora cinnamomi, P. nicotianae and Rhizoctonia solani. The high percentage of total isolates showing antagonistic properties (13%) and their common chitinase and β-glucanase activities indicate that the cell wall constituents of yeasts and macrofungi that proliferate in these compost media may have become a substrate that favours the establishment of antagonistic bacteria to soil-borne fungal pathogens. The selected bacterial strains were further evaluated for their suppressiveness to tomato crown and root rot disease caused by FORL. A total of six rhizospheric isolates, related to known members of the genera Bacillus, Lysinibacillus, Enterobacter and Serratia and one RAE associated with Alcaligenes faecalis subsp. were selected, showing statistically significant decrease of plant disease incidence. Inhibitory effects of extracellular products of the most effective rhizospheric biocontrol agent, Enterobacter sp. AR1.22, but not of the RAE Alcaligenes sp. AE1.16 were observed on the growth pattern of FORL. Furthermore, application of cell-free culture extracts, produced by Enterobacter sp. AR1.22, to tomato roots led to plant protection against FORL, indicating a mode of biological control action through antibiosis.

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References

  • Ajithkumar B, Ajithkumar VP, Iriye R, Doi Y, Sakai T (2003) Spore-forming Serratia marcescens subsp. sakuensis subsp. nov., isolated from a domestic wastewater treatment tank. Int J Syst Evol Microbiol 53:253–258

    Article  CAS  PubMed  Google Scholar 

  • Amaral C, Lucas MS, Coutinho J, Crespi AL, Anjos MD, Pais C (2008) Microbiological and physicochemical characterization of olive mill wastewaters from a continuous olive mill in Northeastern Portugal. Bioresour Technol 99:7215–7223

    Article  CAS  PubMed  Google Scholar 

  • Arlorio M, Ludwig A, Boller T, Bonfante P (1992) Inhibition of fungal growth by plant chitinases and β-1, 3-glucanases. Protoplasma 171:34–43

    Article  CAS  Google Scholar 

  • Ben Sassi A, Boularbah A, Jaouad A, Walker G, Boussaid A (2006) A comparison of Olive oil Mill Wastewaters (OMW) from three different processes in Morocco. Process Biochem 41:74–78

    Article  CAS  Google Scholar 

  • Bonanomi G, Antignani V, Pane C, Scala F (2007) Suppression of soilborne fungal diseases with organic amendments. J Plant Pathol 89:311–324

    Google Scholar 

  • Borrero C, Ordovás J, Trillas MI, Avilés M (2006) Tomato Fusarium wilt suppressiveness. The relationship between the organic plant growth media and their microbial communities as characterised by Biolog®. Soil Biol Biochem 38:1631–1637

    Article  CAS  Google Scholar 

  • Broglie K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S, Mauvais CJ, Broglie R (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254:1194–1197

    Article  CAS  PubMed  Google Scholar 

  • Bruce A, Srinivasan U, Staines HJ, Highley TL (1995) Chitinase and lamarinase production in liquid culture of Trichoderma spp and their role in biocontrol of wood decay fungi. Int Biodeterior Biodegrad 35:337–353

    Article  CAS  Google Scholar 

  • Brurberg MB, Nes IF, Eijsink VGH (1996) Comparative studies of chitinases A and B from Serratia marcescens. Microbiology 142:1581–1589

    Article  CAS  PubMed  Google Scholar 

  • Castric PA (1975) Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol 21:613–618

    Article  CAS  PubMed  Google Scholar 

  • Chae DH, De Jin R, Hwangbo H, Kim YW, Kim YC, Park RD, Krishnan HB, Kim KY (2006) Control of late blight (Phytophthora capsici) in pepper plant with a compost containing multitude of chitinase-producing bacteria. Biocontrol 51:339–351

    Article  Google Scholar 

  • Chet I, Ordentlich A, Shapira R, Oppenheim A (1990) Mechanisms of biocontrol of soil-borne plant pathogens by rhizobacteria. Plant Soil 129:85–92

    Article  Google Scholar 

  • Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR). Microbiol Res 164:493–513

    Article  CAS  PubMed  Google Scholar 

  • Chung YR, Hoitink HAH, Lipps PF (1988) Interactions between organic-matter decomposition level and soilborne disease severity. Agric Ecosyst Environ 24:183–193

    Article  Google Scholar 

  • Coorevits A, De Jonghe V, Vandroemme J, Reekmans R, Heyrman J, Messens W, De Vos P, Heyndrickx M (2008) Comparative analysis of the diversity of aerobic spore-forming bacteria in raw milk from organic and conventional dairy farms. Syst Appl Microbiol 31:126–140

    Article  CAS  PubMed  Google Scholar 

  • Dahiya N, Tewari R, Tiwari R, Hoondal G (2005) Production of an antifungal chitinase from Enterobacter sp. NRG4 and its application in protoplast production. World J Microbiol Biotechnol 21:1611–1616

    Article  CAS  Google Scholar 

  • De la Cruz J, Rey M, Lora JM, Hidalgo-Gallego A, Domınguez F, Pintor-Toro JA, Llobell A, Benitez T (1993) Carbon source control on β-glucanases, chitobiase and chitinase from Trichoderma harzianum. Arch Microbiol 159:316–322

    Article  Google Scholar 

  • Dunn AK, Stabb EV (2005) Culture-independent characterization of the microbiota of the ant lion Myrmeleon mobilis (Neuroptera: Myrmeleontidae). Appl Environ Microbiol 71:8784–8794

    Article  CAS  PubMed  Google Scholar 

  • Erhart E, Burian K, Hartl W, Stich K (1999) Suppression of Pythium ultimum by biowaste composts in relation to compost microbial biomass, activity and content of phenolic compounds. J Phytopathol 147:299–305

    CAS  Google Scholar 

  • Fernandez-Caballero C, Romero I, Goi O, Escribano MI, Merodio C, Sanchez-Ballesta MT (2009) Characterization of an antifungal and cryoprotective class I chitinase from table grape berries (Vitis vinifera Cv. Cardinal). J Agric Food Chem 57:8893–8900

    Article  CAS  PubMed  Google Scholar 

  • Garbeva P, van Veen JA, van Elsas JD (2004) Assessment of the diversity, and antagonism towards Rhizoctonia solani AG3, of Pseudomonas species in soil from different agricultural regimes. FEMS Microbiol Ecol 47:51–64

    Article  CAS  PubMed  Google Scholar 

  • Grimont PAD, Grimont F (1984) Genus Serratia Bizio 1823, 288AL. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. The Williams & Wilkins Co, Baltimore, pp 477–484

    Google Scholar 

  • Gupta R, Saxena RK, Chaturvedi P, Virdi JS (1995) Chitinase production by Streptomyces viridificans: its potential in fungal cell wall lysis. J Appl Bacteriol 78:378–383

    CAS  PubMed  Google Scholar 

  • Hoffmann H, Stindl S, Stumpf A, Mehlen A, Monget D, Heesemann J, Schleifer KH, Roggenkamp A (2005) Description of Enterobacter ludwigii sp. nov., a novel Enterobacter species of clinical relevance. Syst Appl Microbiol 28:206–212

    Article  CAS  PubMed  Google Scholar 

  • Hoitink HAJ, Boehm MJ (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annu Rev Phytopathol 37:427–446

    Article  CAS  PubMed  Google Scholar 

  • Hoitink HAL, Stone AG, Grebus ME (1996) Suppression of plant diseases by composts. In: de Bertoldi M (ed) The science of composting. Blackie Academic and Professional, Glasgow, pp 373–381

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21–132

    Google Scholar 

  • Jung WJ, An KN, Jin YL, Park RD, Lim KT, Kim KY, Kim TH (2003) Biological control of damping-off caused by Rhizoctonia solani using chitinase-producing Paenibacillus illinoisensis KJA-424. Soil Biol Biochem 35:1261–1264

    Article  CAS  Google Scholar 

  • Karpouzas DG, Rousidou C, Papadopoulou KK, Bekris F, Zervakis GI, Singh B, Ehaliotis C (2009) Effect of continuous olive mill wastewater applications, in the presence and absence of N fertilization, on the structure of rhizosphere-soil fungal communities. FEMS Microbiol Ecol 70:56–69

    Google Scholar 

  • Kavroulakis N, Ehaliotis C, Ntougias S, Zervakis GI, Papadopoulou KK (2005) Local and systemic resistance against fungal pathogens of tomato plants elicited by a compost derived from agricultural residues. Physiol Mol Plant Pathol 66:163–174

    Article  Google Scholar 

  • Kersters K, De Ley J (1984) Genus Alcaligenes Castellani and Chalmers 1919, 936AL. In: Krieg NR, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 1. The Williams & Wilkins Co., Baltimore, pp 361–373

    Google Scholar 

  • Lim H-S, Kim Y-S, Kim S-D (1991) Pseudomonas stutzeri YPL-1 genetic transformation and antifungal mechanism against Fusarium solani, an agent of plant root rot. Appl Environ Microbiol 57:510–516

    CAS  PubMed  Google Scholar 

  • Lorito M, Di Pietro A, Hayes CK, Woo SL, Harman GE (1993) Antifungal, synergistic interaction between chitinolytic enzymes from Trichoderma harzianum and Enterobacter cloacae. Mol Plant Pathol 83:721–728

    CAS  Google Scholar 

  • Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combination of chitinase and β-1, 3 glucanase. Plant Physiol 88:936–942

    Article  CAS  PubMed  Google Scholar 

  • McKellar ME, Nelson EB (2003) Compost-induced suppression of Pythium damping-off is mediated by fatty-acid-metabolizing seed-colonizing microbial communities. Appl Environ Microbiol 69:452–460

    Article  CAS  PubMed  Google Scholar 

  • Morrissey RF, Dugan EP, Koths JS (1976) Chitinase production by an Arthrobacter sp. lysing cells of Fusarium roseum. Soil Biol Biochem 8:23–28

    Article  CAS  Google Scholar 

  • Nagarajkumar M, Bhaskaran R, Velazhahan R (2004) Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol Res 159:73–81

    Article  CAS  PubMed  Google Scholar 

  • Noble R, Coventry E (2005) Suppression of soil-borne plant diseases with composts: a review. Biocontrol Sci Technol 15:3–20

    Article  Google Scholar 

  • Ntougias S, Zervakis GI, Kavroulakis N, Ehaliotis C, Papadopoulou KK (2004) Bacterial diversity in spent mushroom compost assessed by amplified rDNA restriction analysis and sequencing of cultivated isolates. Syst Appl Microbiol 27:746–754

    Article  CAS  PubMed  Google Scholar 

  • Ntougias S, Zervakis GI, Ehaliotis C, Kavroulakis N, Papadopoulou KK (2006) Ecophysiology and molecular phylogeny of bacteria isolated from alkaline two-phase olive mill wastes. Res Microbiol 157:376–385

    Article  CAS  PubMed  Google Scholar 

  • Ntougias S, Papadopoulou KK, Zervakis GI, Kavroulakis N, Ehaliotis C (2008) Suppression of soil-borne pathogens of tomato by composts derived from agro-industrial wastes abundant in Mediterranean regions. Biol Fertil Soils 44:1081–1090

    Article  Google Scholar 

  • Ordentlich A, Elad Y, Chet I (1988) The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii. Phytopathology 78:84–88

    CAS  Google Scholar 

  • Perez-Piqueres A, Edel-Hermann V, Alabouvette C, Steinberg C (2006) Response of soil microbial communities to compost amendments. Soil Biol Biochem 38:460–470

    Article  CAS  Google Scholar 

  • Priest FG, Aquino De Muro M, Kaji D (1994) Systematics of insect pathogenic bacilli: uses in strain identification and isolation of novel pathogens. In: Priest FG, Ramos-Cormenzana A, Tindall BJ (eds) Bacterial diversity and systematics. Plenum, New York, pp 275–296

    Google Scholar 

  • Raddadi N, Cherif A, Ouzari H, Marzorati M, Brusetti L, Boudabous A, Daffonchio D (2007) Bacillus thuringiensis beyond insect biocontrol: plant growth promotion and biosafety of polyvalent strains. Ann Microbiol 57:481–494

    Article  CAS  Google Scholar 

  • Roberts DP, JrNM S, Maloney AP, Nelson EB, Schaff DA (1994) Role of colonization in biocontrol: studies with Enterobacter cloacae. Plant Sci 101:83–89

    Article  Google Scholar 

  • Robinson SP, Jacobs AK, Dry IB (1997) A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol 114:771–778

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method—a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, Feitelson J, Zeigler DR, Dean DH (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62:775–806

    CAS  PubMed  Google Scholar 

  • Senthilkumar M, Swarnalakshmi K, Govindasamy V, Lee YK, Annapurna K (2009) Biocontrol potential of soybean bacterial endophytes against charcoal rot fungus, Rhizoctonia bataticola. Curr Microbiol 58:288–293

    Article  CAS  PubMed  Google Scholar 

  • Shoebitz M, Ribaudo CM, Pardo MA, Cantore ML, Ciampi L, Curá JA (2009) Plant growth promoting properties of a strain of Enterobacter ludwigii isolated from Lolium perenne rhizosphere. Soil Biol Biochem 41:1768–1774

    Article  CAS  Google Scholar 

  • Siddiqui Y, Meon S, Ismail MR, Ali A (2008) Trichoderma-fortified compost extracts for the control of choanephora wet rot in okra production. Crop Prot 27:385–390

    Article  Google Scholar 

  • Someya N, Nakajima M, Akutsu K (2005) Potential of an antagonistic bacterium Serratia marcescens strain B2 for the biological control of cucumber damping-off disease. Biocontrol Sci 10:101–104

    Google Scholar 

  • Streichsbier F, Messner K, Wessely M, Rohr M (1982) The microbiological aspects of grape marc humification. Eur J Appl Microbiol Biotechnol 14:182–186

    Article  Google Scholar 

  • Strohl WR (1997) Industrial antibiotics: today and the future. In: Strohl WR (ed) Biotechnology of antibiotics. Marcel Dekker Ins, New York, pp 3–35

    Google Scholar 

  • Termorshuizen AJ, van Rijn E, van der Gaag DJ, Alabouvette C, Chen Y, Lagerlöf J, Malandrakis AA, Paplomatas EJ, Rämert B, Ryckeboer J, Steinberg C, Zmora-Nahum S (2007) Suppressiveness of 18 composts against 7 pathosystems: variability in pathogen response. Soil Biol Biochem 38:2461–2477

    Article  CAS  Google Scholar 

  • Trillas MI, Casanova E, Cotxarrera L, Ordovás J, Borrero C, Avilés M (2006) Composts from agricultural waste and the Trichoderma asperellum strain T-34 suppress Rhizoctonia solani in cucumber seedlings. Biol Control 39:32–38

    Article  Google Scholar 

  • Vaidya RJ, Shah IM, Vyas PR, Chhatpar HS (2001) Production of chitinase and its optimization from a novel isolate Alcaligenes xylosoxydans: potential in antifungal biocontrol. World J Microbiol Biotechnol 17:691–696

    Article  CAS  Google Scholar 

  • Van de Peer Y, De Wachter R (1993) TREECON: a software package for the construction and drawing of evolutionary trees. Comput Appl Biosci 9:77–182

    Google Scholar 

  • van Dijk K, Nelson EB (2000) Fatty acid competition as a mechanism by which Enterobacter cloacae suppresses Pythium ultimum sporangium germination and damping-off. Appl Environ Microbiol 66:5340–5347

    Article  PubMed  Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  CAS  Google Scholar 

  • Vierheilig H, Alt M, Neuhaus JM, Boller T, Wiemken A (1993) Colonization of transgenic Nicotiana sylvestris plants expressing different forms of Nicotiana tabacum chitinase by the root pathogen Rhizoctonia solani and by the mycorrhizal symbiont Glomus mosseae. Mol Plant Microbe Interact 6:261–264

    CAS  Google Scholar 

  • Voisard C, Keel C, Haas D, Defago G (1989) Cyanide production by Pseudomonas fluorescens helps suppress black root rot of tobacco under gnotobiotic conditions. EMBO J 8:351–358

    CAS  PubMed  Google Scholar 

  • Walsh GA, Murphy RA, Killeen GF, Headon DR, Power RF (1995) Technical note: detection and quantification of supplemental fungal beta-glucanase activity in animal feed. J Anim Sci 73:1074–1076

    PubMed  Google Scholar 

  • Weller DM, Raaijmakers JM, McSpadden Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348

    Article  CAS  PubMed  Google Scholar 

  • Wilson K (1992) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (eds) Short protocols in molecular biology. Wiley, New York, pp 2-10–2-11

    Google Scholar 

  • Zhang W, Han DY, Dick WA, Davis KR, Hoitink HAJ (1998) Compost and compost water extract-induced systemic acquired resistance in cucumber and Arabidopsis. Phytopathology 88:450–455

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Menia Kardimaki for excellent technical assistance. This study was partially funded by the RECOVEG project (E.U., QLRT-2000-01458) and the Greek Ministry of Development Secretariat for Research and Technology (EPAN FP 66).

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Author notes

  1. Maria I. Besi

    Present address: Department of Disease and Stress Biology, John Innes Centre, Colney Lane, Norwich, NR4 7UH, UK

  2. Georgios I. Zervakis

    Present address: Laboratory of Agricultural Microbiology, Agricultural University of Athens, Iera Odos 75, Athens, 118 55, Greece

Authors and Affiliations

  1. Institute of Kalamata, National Agricultural Research Foundation, Lakonikis 87, Kalamata, 24100, Greece

    Nektarios Kavroulakis, Spyridon Ntougias, Pelagia Katsou, Athanasia Damaskinou & Georgios I. Zervakis

  2. Department of Biochemistry and Biotechnology, University of Thessaly, Ploutonos 26 & Aeolou, Larisa, 41221, Greece

    Maria I. Besi & Kalliope K. Papadopoulou

  3. Soils and Agricultural Chemistry Laboratory, Agricultural University of Athens, Iera Odos 75, Athens, 118 55, Greece

    Constantinos Ehaliotis

  4. Institute of Chania, National Agricultural Research Foundation, 73100, Chania, Crete, Greece

    Nektarios Kavroulakis

  5. Laboratory of Wastewater Management and Treatment, Department of Environmental Engineering, Democritus University of Thrace, Vas. Sofias 12, 67100, Xanthi, Greece

    Spyridon Ntougias

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Kavroulakis, N., Ntougias, S., Besi, M.I. et al. Antagonistic bacteria of composted agro-industrial residues exhibit antibiosis against soil-borne fungal plant pathogens and protection of tomato plants from Fusarium oxysporum f.sp. radicis-lycopersici . Plant Soil 333, 233–247 (2010). https://doi.org/10.1007/s11104-010-0338-x

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