Skip to main content
Log in

Biocontrol and plant growth-promoting potentiality of bacteria isolated from compost extract

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

The use of compost extracts is steadily increasing, offering an attractive way for plant growth enhancement and disease management replacing chemical pesticides. In this study, potential mechanisms involved in plant growth promotion and suppressive activity against fungal diseases, of a compost extract produced from poultry manure/olive husk compost, were investigated. Results of physico-chemical and microbiological investigations showed high ability to reduce Fusarium oxysporum, Alternaria alternata, Aspergillus niger and Botrytis cinerea growth. The suppressive ability detected using confrontation test and the phytostimulatory effect tested on tomato seeds were related mainly to its microbial population content. Among 150 bacterial strains, isolated from the compost extract, 13 isolates showed antifungal activity against the four tested plant pathogenic fungi. Their identification based on 16S rRNA gene sequence revealed they belonged to different species of the genus Bacillus, Alcaligenes, Providencia and Ochrobactrum. When tested for their ability to produce cell wall degradation enzymes using specific media, the majority of the 13 isolates were shown to synthesize proteases, lipases and glucanases. Similarly, the best part of them showed positive reaction for plant growth promoting substances liberation, biosurfactant production and biofilm formation. In vivo tests were carried out using tomato seeds and fruits and proved that 92% of strains improved tomato plants vigor indexes when compared to the control and 6 among them were able to reduce decay severity caused by B. cinerea over 50%. Principal component analysis showed an important correlation between in vitro and in vivo potentialities and that Bacillus siamensis CEBZ11 strain was statistically the most effective strain in protecting tomato plants from gray mould disease. This study revealed the selected strains would be useful for plant pathogenic fungi control and plant growth promotion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

References

  • Abdel-Mawgoud AM, Aboulwafa MM, Hassouna NAH (2008) Optimization of surfactin production by Bacillus subtilis isolate BS5. App Biochem Biotechnol 150:305–325

    CAS  Google Scholar 

  • Abdul-Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria. Crop Sci 13:630–633

    Google Scholar 

  • Adegunloye DV, Adetuyi FC, Akinyosoye FA, Doyeni MO (2007) Microbial analysis of compost using cowdung as booster. Pak J Nutr 6:506–510

    Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria. Current perspective J K S Univ Sci 26:1–20

    Google Scholar 

  • Ahmad I, Ahmad F, Khan MS (2008) Screening of free living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    CAS  PubMed  Google Scholar 

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12(1):39–45

    CAS  Google Scholar 

  • Amaresan N, Jayakumar V, Kumar K, Thajuddin N (2019) Biocontrol and plant growth-promoting ability of plant-associated bacteria from tomato (Lycopersicum esculentum) under field condition. Microb Pathog 136:103713

    CAS  PubMed  Google Scholar 

  • Arshad M, Frankenberger WT (1991) Microbial production of plant hormones. Plant Soil 133:1–8

    CAS  Google Scholar 

  • Ayangbenro AS, Babalola OO (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 14:94

    PubMed Central  Google Scholar 

  • Berrada I, Benkhemmar O, Swings J, Bendaou N, Amar M (2012) Selection of halophilic bacteria for biological control of tomato grey mould caused by Botrytis cinerea. Phytopathol Mediterr 51(3):625–630

    CAS  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    CAS  PubMed  Google Scholar 

  • Castano R, Borrero C, Aviles M (2011) Organic matter fractions by SP-MAS 13C NMR and microbial communities involved in the suppression of Fusarium wilt in organic growth media. Biol Control 58:286–293

    Google Scholar 

  • Chakraborty U, Chakraborty BN, Basnet M, Chakraborty AP (2009) Evaluation of Ochrobactrum anthropi TRS-2 and its talc based formulation for enhancement of growth of tea plants and management of brown root rot disease. J Appl Microbiol 107(2):625–634

    CAS  PubMed  Google Scholar 

  • Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Envi Microbiol 53(2):22

    Google Scholar 

  • Curlango-Rivera G, Pew T, VanEtten HD, Zhongguo X, Yu N, Hawes MC (2013) Measuring root disease suppression in response to a compost water extract. Phytopathology 3:255–260

    Google Scholar 

  • Du N, Shi L, Yuan Y, Sun J, Shu S, Guo S (2017) Isolation of a potential biocontrol agent Paenibacillus polymyxa NSY50 from vinegar waste compost and its induction of host defense responses against Fusarium wilt of cucumber. Microbiol Res 202:1–10

    PubMed  Google Scholar 

  • Ekundayo EA, Detuyi FC, Ekundayo FO (2011) In vitro antifungal activities of bacteria associated with maize husks and cobs. Res J Microbiol 6:418–424

    Google Scholar 

  • El-Masry MH, Khalil AI, Hassouna MS, Ibrahim HAA (2002) In situ and in vitro suppressive effect of agricultural composts and their water extracts on some plant pathogenic fungi. World J Microbiol Biotechnol 18:551–558

    CAS  Google Scholar 

  • Flemming HC, Wingender J (2001) Relevance of microbial extracellular polymeric substances (EPSs). Part I: structural and ecological aspects. Water Sci Technol 43:1–8

    CAS  PubMed  Google Scholar 

  • Gholami A, Shahsavani S, Nezarat S (2009) The effect of plant growth promoting rhizobacteria (PGPR) on germination, seedling growth and yield of maize. Int J Biol Life Sci 1(1):35–40

    Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (2012):1–15

    Google Scholar 

  • Gordon AS, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goswami M, Deka S (2019) Biosurfactant production by a rhizosphere bacteria Bacillus altitudinis MS16 and its promising emulsification and antifungal activity. Colloids Surf B 178:285–296

    CAS  Google Scholar 

  • Hachicha S, Sallemi F, Medhioub K, Hachicha R, Ammar E (2008) Quality assessment of composts prepared with olive mill wastewater and agricultural wastes”. Waste Manag 28:2593–2603

    CAS  PubMed  Google Scholar 

  • Hmouni A, Hajlaoui MR, Mlaiki A (1996) Résistance de Botrytis cinerea aux benzimidazoles et aux dicarboximides dans les cultures abritées de tomate en Tunisie. OPPE Bull 26:697–705

    Google Scholar 

  • Hussain K, Hameed S, Shahid M, Amanat A, Iqbal J, Hahn D (2015) First report of Providencia vermicola strains characterized for enhanced rapeseed growth attributing parameters. Int J Agric Biol 17(6):1110–1116

    CAS  Google Scholar 

  • Imran A, Saadalla MJA, Khan SU, Mirza MS, Malik KA, Hafeez FY (2014) Ochrobactrum sp. Pv2Z2 exhibits multiple traits of plant growth promotion, biodegradation and N-acyl-homoserine-lactone quorum sensing. Ann Microbiol 64(4):1797–1806

    CAS  Google Scholar 

  • Indiragandhi P, Anandham R, Madhaiyan M, Sa TM (2008) Characterization of plant growth-promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Curr Microbiol 56:327–333

    CAS  PubMed  Google Scholar 

  • Japanese Standards Association (1995) Wastewater treatment. In: Japanese Standards Association (eds) JIS handbook. Environmental Technology, Tokyo, pp 553–638

    Google Scholar 

  • Kilani-Feki O, Khedher SB, Dammak M, Kamoun A, Jabnoun-Khiareddine H, Daami-Remadi M, Tounsi S (2016) Improvement of antifungal metabolites production by Bacillus subtilis V26 for biocontrol of tomato postharvest disease. Biol Control 95:73–82

    CAS  Google Scholar 

  • Koné SB, Dionne A, Tweddell RJ, Antoun H, Avis TJ (2010) Suppressive effect of non-aerated compost teas on foliar fungal pathogens of tomato”. Biol Control 52:167–173

    Google Scholar 

  • Lapwood DH, Read P, Spokes J (1984) Methods for assessing the susceptibility of potato tubers of different cultivars to rotting by Erwinia carotovora subspecies atroseptica and carotovora. Plant Pathol 33:13–20

  • Li ZY, Hu Y, Huang YQ, Huang Y (2007) Isolation and phylogenetic analysis of the biologically active bacteria associated with three South China Sea sponges. Microbiol 76(4):494–499

    CAS  Google Scholar 

  • Lim HS, Kim SD (1994) The production and enzymatic properties of extracellular chitinase from Pseudomonas stutzeri YPL1 as a biocontrol agent. J Microbiol Biotechnol 4:134–140

    CAS  Google Scholar 

  • Lin Y, Du D, Si C, Zhao Q, Li Z, Li P (2014) Potential biocontrol Bacillus sp. strains isolated by an improved method from vinegar waste compost exhibit antibiosis against fungal pathogens and promote growth of cucumbers. Biol Control 71:7–15

    Google Scholar 

  • Lu X, Liu SF, Yue L, Zhao X, Zhang YB, Xie ZK, Wang RY (2018) Epsc involved in the encoding of exopolysaccharides produced by Bacillus velezensis FZB42 act to boost the drought tolerance of Arabidopsis thaliana. Int J Mol Sci 19(12):3795

    PubMed Central  Google Scholar 

  • Manios T (2004) The composting potential of different organic solid wastes: experience from the island of Crete. Environ Int 29:1079–1089

    CAS  PubMed  Google Scholar 

  • Masmoudi F, Khedher SB, Kamoun A, Zouari N, Tounsi S, Trigui M (2017) Combinatorial effect of mutagenesis and medium component optimization on Bacillus amyloliquefaciens antifungal activity and efficacy in eradicating Botrytis cinerea. Microbiol Res 197:29–38

    PubMed  Google Scholar 

  • Masmoudi F, Abdelmalek N, Tounsi S, Dunlap CA, Trigui M (2019) Abiotic stress resistance, plant growth promotion and antifungal potential of halotolerant bacteria from a Tunisian solar saltern. Microbiol Res 229:126–331

    Google Scholar 

  • Mehta CM, Palni U, Franke-Whittle IH, Sharma AK (2014) Compost: its role, mechanism and impact on reducing soil-borne plant diseases. Waste Manag 34(3):607–622

    CAS  Google Scholar 

  • Meng Q, Jiang H, Hao JJ (2016) Effects of Bacillus velezensis strain BAC03 in promoting plant growth. Biol Control 98:18–26

    CAS  Google Scholar 

  • Moterle LM, dos Santos R, Scapim CA, Lucca e Braccini AD, Bonato C., Conrado T (2011). Effect of plant growth regulator on germination and vigor of soybean seeds. Revista Ceres 58(5):651–660

  • Murata T, Iida T, Shiomi Y, Tagomori K, Akeda Y, Yanagihara I, Mushiake S, Ishiguro F, Honda T (2001) A large outbreak of foodborne infection attributed to Providencia alcalifaciens. J Infect Dis 184:1050–1055

    CAS  PubMed  Google Scholar 

  • Okumu OO, Muthomi JW, Ojiem J, Narla R, Nderitu JH (2019) Effect of legume extracts on germination, seedling health of beans (Phaseolus vulgaris L.) and soil microorganisms. Int J Plant Soil Sci 28(1):1–13

    Google Scholar 

  • On A, Wong F, Ko Q, Tweddell RJ, Antoun H, Avis TJ (2015) Antifungal effects of compost tea microorganisms on tomato pathogens. Biol Control 80:63–69

    Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Ann Rev Microbiol 54:49–79

    Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370

    CAS  Google Scholar 

  • Praveen Kumar D, Anupama PD, Singh RK, Thenmozhi R, Nagasathya A, Thajuddin N, Paneerselvam A (2012) Performance studies of free-living tomato (Lycopersiconexculentum L.) rhizospheric Bacillus for their multiple plant growth promoting activity. J Soil Sci Environ Manage 3:142–153

    Google Scholar 

  • Priyanka R, Nakkeeran S (2019) Ochrobactrum ciceri mediated induction of defense genes and antifungal metabolites enhance the biocontrol efficacy for the management of Botrytis leaf blight of Lilium under protected conditions. J Plant Pathol 101(2):323–337

    Google Scholar 

  • Radhakrishnan R, Hashem A, Abd_Allah EF (2017) Bacillus Front Physiol 8:667

    PubMed  Google Scholar 

  • Ramadoss D, Lakkineni VK, Bose P, Ali S, Annapurna K (2013) Mitigation of salt stress in wheat seedlings by halotolerant bacteria isolated from saline habitats. SpringerPlus 2:6

    PubMed  PubMed Central  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aus J Plant Physiol 28(9):897–906

    Google Scholar 

  • Sachdev DP, Cameotra SS (2013) Biosurfactants in agriculture. Appl Microbiol Biotechnol 97(3):1005–1016

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santoa SN, Oliveira LKX, de Melo IS, da Silva Velozo E, de Abreu Roque MR (2011) Antifungal activity of bacterial strains from the rhizosphere of Stachytarpheta crassifolia. Afr J Biotechnol 10(25):4996–5000

    Google Scholar 

  • Sariwati A, Purnomo AS, Kamei I (2017) Abilities of Co-cultures of Brown-Rot Fungus Fomitopsis pinicola and Bacillus subtilis on Biodegradation of DDT. Curr Microbiol 74(9):1068–1075

    CAS  PubMed  Google Scholar 

  • Sarwar M, Arshad M, Martens DA, Frankenberger JWT (1992) Tryptophan-dependent biosynthesis of auxins in soil. Plant Soil 147:207–215

    CAS  Google Scholar 

  • Sayyed ZR, Gangurde NS, Patel RP, Joshi SA, Chincholkar SB (2010) Siderophore Production by Alcaligenes faecalis and its application for Growth Promotion in Arachis hypogea. Indian J Biotechnol 9:302–307

    CAS  Google Scholar 

  • Shekhar S, Sundaramanickam A, Balasubramanian T (2015) Biosurfactant producing microbes and their potential applications: a review. Crit Rev Environ Sci Technol 45(14):1522–1554

    CAS  Google Scholar 

  • Siddiqui Y, Meon S, Ismail R, Rahmani M (2009) Bio-potential of compost tea from agro-waste to suppress Choanephora cucurbitarum L. the causal pathogen of wet rot of okra. Biol Control 49:38–44

    Google Scholar 

  • Sierrea G (1957) A simple method for the detection of lipolytic activity of micro-organisms and some observations on the influence of the contact between cells and fatty substrates. Anton Van Leeuw 23(1):15–22

    Google Scholar 

  • Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerharelt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and Molecular Bacteriology. American Society of Microbiology, Washington DC, pp 607–654

    Google Scholar 

  • Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol 3:a00143

    Google Scholar 

  • St. Martin CCG, Dorinvil W, Brathwaite RAI, Ramsubhag A (2012) Effects and relationships of compost type, aeration and brewing time on compost tea properties, efficacy against Pythium ultimum, phytotoxicity and potential as a nutrient amendment for seedling production. Biol Agric Hort 28:185–205

    Google Scholar 

  • Tan S, Jiang Y, Song S, Huang J, Ling N, Xu Y, Shen Q (2013) Two Bacillus amyloliquefaciens strains isolated using the competitive tomato root enrichment method and their effects on suppressing Ralstonia solanacearum and promoting tomato plant growth. Crop Prot 43:134–140

    Google Scholar 

  • Tanimoto E (2005) Regulation of root growth by plant hormones roles for auxin and gibberellin. Crit Rev Plant Sci 24:249–265

    CAS  Google Scholar 

  • Termorshuizen AJ, Van Rijn E, Van Der Gaag DJ, Alabouvette C, Chen Y, Lagerlöf J, Malandrakisf AA, Paplomatasf EJ, Rämerte B, Ryckeboerg J, Steinberg C, Zmora-Nahumd S (2006) Suppressiveness of 18 composts against 7 pathosystems: variability in pathogen response. Soil Biol Biochem 38(8):2461–2477

    CAS  Google Scholar 

  • UNIT Recycled Organics (2003) Producing Quality Compost: Operation and management guide to support the consistent production of quality compost and products containing recycled organics. The University of New South Wales, Sydney

    Google Scholar 

  • Wang L, Jin P, Wang J, Jiang L, Zhang S, Gong H, Zheng Y (2015) In vitro inhibition and in vivo induction of defense response against Penicillium expansum in sweet cherry fruit by postharvest applications of Bacillus cereus AR156. Postharvest Biol Technol 101:15–17

  • Willumsen PAE, Karlson U (1997) Screening of bacteria, isolated from PAH contaminated soils, for production of biosurfactants and bioemulsifiers. Biodegradation 7:415–423

    Google Scholar 

  • Xu D, Raza W, Yu G, Zhao Q, Shen Q, Huang Q (2012) Phytotoxicity analysis of extracts from compost and their ability to inhibit soil-borne pathogenic fungi and reduce root-knot nematodes. W J Microbiol Biotechnol 28:1193–1201

    Google Scholar 

  • Xu BH, Ye ZW, Zheng QW, Wei T, Lin JF, Guo LQ (2018) Isolation and characterization of cyclic lipopeptides with broad-spectrum antimicrobial activity from Bacillus siamensis JFL15. 3 Biotech 8(10):444

    PubMed  PubMed Central  Google Scholar 

  • Yakhin OI, Lubyanov AA, Yakhin IA, Brown PH (2017) Biostimulants in plant science: a global perspective. Front Plant Sci 7:2049

  • Zheng YN, Wang J, Pan RN, Wang S, Duo LA, Zhao S (2016) Effects of foliar spraying complex microbial inoculum from compost on seed germination and seedling growth of turfgrass. Seed 7:6

    Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Rania Bahloul, University of Sfax-Tunisia, for proofreading the manuscript.

Funding

This work was supported by grants from the Tunisian Ministry of Higher Education and Scientific Research.

Author information

Authors and Affiliations

Authors

Contributions

Conceived and designed the experiments: IZ, MT, ST and KM. Performed the experiments: IZ. Analyzed the data: IZ,MT,ST and FM. Wrote the paper: IZ,FM,MT and ST. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Fatma Masmoudi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests regarding the present study.

Ethical approval

The authors declare no ethical conflicts.

Consent to participate

Authors declare that they have consented to participate in the manuscript and publish it.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zouari, I., Masmoudi, F., Medhioub, K. et al. Biocontrol and plant growth-promoting potentiality of bacteria isolated from compost extract. Antonie van Leeuwenhoek 113, 2107–2122 (2020). https://doi.org/10.1007/s10482-020-01481-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-020-01481-8

Keywords

Navigation