Abstract
Twelve bacterial strains (GJ01 to GJ12), isolated from an oil-contaminated soil, were characterized through different biochemical, morphological, and molecular technique and analyzed by different screening methods to choose the best biosurfactant producing strain. Only GJ-01 strain exhibited significant biosurfactant activity, while the other strains exhibited partial activity. Molecular identification through 16S rRNA technique identified GJ-01 as a Bacillus siamensis-AMU03. The effect of the cultural filtrate tested under in vitro study against Rhizoctonia solani and Fusarium oxysporum, with the highest reduction of mycelial growth in dual culture method (89.40% and 90.20% respectively). Both in food poisoning method as well as pathogenicity test, the bioagent was able to inhibit the growth of both the pathogens successfully at 3% concentration, and that was mainly due to volatile metabolites such as surfactin, fengycin and iturin, which were identified and analysed through Liquid chromatography-mass spectrometry. These findings indicated that AMU03 strain had a promising eco-friendly and bio-safe approach to cope against soil-borne and post-harvest pathogens of seed tubers.
Similar content being viewed by others
References
Adesina MF, Lembke A, Costa R, Speksnijder A, Smalla K (2007) Screening of bacterial isolates from various European soils for in vitro antagonistic activity towards Rhizoctonia solani and Fusarium oxysporum: site-dependent composition and diversity revealed. Soil Biol Biochem 39:2818–2828
Akihiro O, Takashi A, Makoto S (1993) Production of the antifungal peptide antibiotic-iturin by Bacillus subtilis NB22 in solid-state fermentation. J Ferment Bioeng 75:23–27
Aleti G, Lehner S, Bacher M, Compant S, Nikolic B, Plesko M (2016) Surfactin variants mediate speciesspecific biofilm formation and root colonization in Bacillus. Environ Microbiol 18:264–2645
Aneja KR (2003) Experiments in Microbiology, Plant Pathology and Biotechnology. New Age International (Pvt.) Ltd, New Delhi
Anonymous (2017) https://www.marketsandmarkets.com/Market-Reports/biosurfactant-market-163644922.html
Arguelles-Arias A, Ongena M, Halimi B, Lara Y, Brans A, Joris B, Fickers P (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microbial Cell Fact 8:63
Arora RK (2005) Efficacy of boric acid spray for control of black scurf in unwashed and washed potato tubers. Potato J 32:183–184
Arora RK, Sharma J, Garg ID, Singh RK, Somani AK (2006) Boric acid for control of tuber borne diseases. Central Potato Research Institute, Shimla, India. Tech Bulletin 35:1–4
Arrebola E, Jacobs R, Korsten L (2010) Iturin A is the principal inhibitor in the biocontrol activity of Bacillus amyloliquefaciensPPCB004 against postharvest fungal pathogens. J Appl Microbiol 108:386–395
Bagri RK, Kumar V, Kumari M (2017) Management of black scurf disease of potato using chemicals Penflufen and Boric acid. Int J Chem Stud 5(4):83–85
Beltran V (2018) Pesticide use: Crop management, yield and environmental impact on potato field in the Netherlands, MSc Thesis Wageningen University: 52
Bodour AA, Maier RM (1998) Application of a modified drop collapse technique for surfactant quantification and screening of biosurfactant- producing microorganisms. J Microbiol Methods 32:273–280
Boruah B, Gogoi M (2013) Plant based natural surfactants. Asian J Home Sci 8(2):759–762
Cavaglieri L, Orlando J, Rodríguez MI, Chulze S, Etcheverry M (2005) Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. Res Microbiol 156:748–754
Chen WC, Juang RS, Wei YH (2015) Applications of a lipopeptide biosurfactant, surfactin, produced by microorganisms. Biochem Eng J 103:158–169
Cooper DG, Goldenberg BG (1987) Surface-active agents from 2 Bacillus species. Appl Environ Microbiol 53:224–229
Coronel-León J, de Grau G, Grau-Campistany A, Farfan M, Rabanal F, Manresa A, Marqués AM (2015) Biosurfactant production by AL 1.1, a Bacillus licheniformis strain isolated from Antarctica production, chemical characterization and properties. Ann Microb. https://doi.org/10.1007/s13213-015-1045-x
Daami-Remadi M, Zammouri S, El Mahjoub M (2008) Relative susceptibility of nine potato (Solanum tuberosum L.) cultivars to artificial and natural infection by Rhizoctonia solani as measured by stem canker severity, black scurf and plant growth, Afr. J Plant Sci Biotech 2:57–66
Das BC, Hazarika DK (2000) Biological management of sheath blight of rice. Indian Phytopathol 53:433–435
De Almeida DG, Soares Da Silva RCF, Luna JM, Rufino RD, Santos VA, Banat IM, Sarubbo LA (2016) Biosurfactants: promising molecules for petroleum biotechnology advances. Front Microbiol 7:1718
Du M, Ren X, Sun Q, Wang Y, Zhang R (2012) Characterization of Fusarium spp. causing potato dry rot in China and susceptibility evaluation of Chinese potato germplasm to the pathogen. Potato Res 55:175–184
Dunlap CA, Schisler DA, Price NP, Vaughn SF (2011) Cyclic lipopeptide profile of three Bacillus subtilis strains; antagonists of Fusarium head blight. J Microbiol 49:603–609
Elkahoui S, Djébali N, Tabbene O, Hadjbrahim A, Mnasri B, Mhamdi R, Limam F (2011) Screening of bacterial isolates collected from marine bio-films for antifungal activity against Rhizoctonia solani. Dynamic Biochemistry, Process Biotechnol. Mol Biol 5(2):1–4
Faltin FJ, Lottmann R, Grosch GB (2004) Strategy to select and assess antagonistic bacteria for biological control of Rhizoctonia solani Ku¨hn. Can J Microbiol 50:811–820
Feng S, Shu C, Wang C, Jiang S, Zhou E (2017) Survival of Rhizoctonia solani AG-1 IA, the causal agent of rice sheath blight, under different environmental conditions. J Phytopathol 165:44–52
Fokkema NJ (1973) The role of saprophytic fungi in antagonism against Derchslerasorokaniana (Helminthosporium sativum) on agar plates and on rye leaves with pollen. Physiol Plant Pathol 3:195–205
Fracchia L, Ceresa C, Franzetti A, Cavallo M, Gandolfi I, Hamme J, Van Banat IM (2014) Industrial applications of biosurfactnats. CRC Press, Atlanta, pp 245–268
Gal-Hemed L, Atanasova M, Komon-Zelazowska IS, Druzhinina A, Viterbo and O Yarden, (2011) Marine isolates of Trichoderma spp. As potential halotolerant agents of biological control for arid-zone agriculture. Appl Environ Microbiol 77(15):5100–5109
Groth DE, Bond JA (2006) Initiation of rice sheath blight epidemics and effects of application timing of azoxystrobin on disease incidence, severity, yield and milling yields. Plant Dis 90:1073–1078
Grover RK, Moore JD (1962) Toximetric studies of fungicides of brown rot organism Sclerotinia fruticola and S. laxa. Phytopathology 52:876–880
Hong Z, Cong B, Tian Y, He Yu, Yang H (2009) Characterization of novel cyclic lipopeptides produced by Bacillus sp. SY27F. Process Biochem 83:206–213
Hussain T (2020a) Bacterial metabolites: a gift from nature for crop protection. The Global Plant Council. https://globalplantcouncil.org/bacterial-metabolites-a-gift-from-nature-for-cropprotection/
Hussain T (2020b) Harnessing natural bio factories against deadly soil fungal pathogens of potato seed tubers: Bacillus subtilis. In: Soil Health case studies-75th anniversary of the Microbiology Society, London, U.K. https://microbiologysociety.org/our-work/75th-anniversary-a-sustainable-future/soil-health/soil-health-case-studies/harnessing-natural-bio-factories.html
Hussain T, Khan AA (2018a) A combination of rapid and easy assays of biosurfactant producing bacteria strain isolated from automobiles repairing workshop in Aligarh. Proc Voronezh State Univ Eng Technol 80(3):153–163
Hussain T, Khan AA (2018b) Biosurfactant weapons-A hidden Weapon against deadly fungal pathogens of potato. Indian Phytopatho Newsletter, vol 1, no 4, p 3. http://storage.unitedwebnetwork.com/files/302/e1291fe55fead86fb1da165f411ab9e2.pdf
Hussain T, Khan AA (2020a) Bacillus subtilis HussainT-AMU and its antifungal activity against Potato black scurf caused by Rhizoctonia solani. Biocatal Agric Biotechnol 23:101433
Hussain T, Khan AA (2020b) Isolation of potential biosurfactant bacteria from railway diesel engine yard soil, its PCR detection and antifungal activity Rhizoctonia solani of potato tuber. Agrica J 9:39–52
Hussain T, Khan AA (2020c) Determining the antifungal activity and characterization of Bacillus siamensis AMU03 against Macrophomina phaseolina (Tassi) Goid. Indian Phytopathol 73:507–516
Hussain T, Akhtar N, Aminedi R, Danish M, Nishat Y, Patel S (2020a) Role of the potent microbial based bio agent and their emerging strategies for the eco-friendly management of Agricultural Phytopathogens. In: Singh J, Yadav AN (eds) Natural bioactive products in sustainable agriculture. Springer, Singapore, pp 45–66. https://doi.org/10.1007/978-981-15-3024-1_14
Hussain T, Singh S, Danish M, Pervez R, Hussain K, Hussain R (2020b) Natural Metabolites an eco-friendly approach to manage plant diseases and for better agricultural farming. In: Singh J, Yadav AN (eds) Natural bioactive products in sustainable agriculture. Springer, Singapore, pp 1–13. https://doi.org/10.1007/978-981-15-3024-1_1e
Hussain T, Haris M, Shakeel A, Khan AA, Khan MA (2020c) Bio-nematicidal activities by culture filtrateof Bacillus subtilisHussainT-AMU: new promising biosurfactantbioagent for the management of Root Galling caused by Meloidogyne incognita. Vegetos 33:229–238
Hussain T, Khan A, Khan M (2021) Biocontrol of soil borne pathogen of potato tuber caused by Rhizoctonia solani through biosurfactant based Bacillus strain. J Nepal Agri Res Council 7(1):54–66. https://doi.org/10.3126/jnarc.v7i1.36921
Jadhav M, Kalme S, Tamboli D, Govindwar S (2011) Rhamnolipid from Pseudomonas desmolyticum NCIM-2112 and its role in the degradation of brown 3REL. J Basic Microbiol 51:385–396
John G, Holt PhD, Peter H Sneath, Noel R Krieg, John G Holt, John G. Holt (1994) Bergey`s Manual of Determinative Bacteriology (9th Edition).ISBN-13: 9780683006032
Khedher SB, Kilani-Feki O, Dammak M, Jabnoun-Khiareddine H, Daami-Remadi M, Tounsi S (2015) Efficacy of Bacillus subtilis V26 as a biological control agent against Rhizoctonia solani on potato. CR Biol. https://doi.org/10.1016/j.crvi.2015.09.005
Kim YT, Park BK, Kim SE, Lee WJ, Moon JS, Cho MS et al (2017) Organization and characterization of genetic regions in Bacillus subtilis subsp. krictiensis ATCC55079 associated with the biosynthesis of iturin and surfactin compounds. PLoS ONE 12:e0188179
Kosaric N (2001) Biosurfactants and their application for soil bioremediation. Food Technol Biotechnol 39:295–304
Krishnaswamy M, Subbuchettiar G, Ravi TK, Panchaksharam S (2008) Biosurfactants: properties, commercial production and application. Curr Sci 94:736–774
Kucuk C, Kivanc M (2003) Isolation of Trichoderma spp. and determination of their antifungal, biochemical and physiological features. Turk J Biol 27:247–253
Kumar A, Raj K (2016) Evaluation of different fungicides against black scurf of potato caused by Rhizoctonia solani. Indian J Plant Protection 44(1):110–115
Lastochkina O, Pusenkova L, Garshina D, Yuldashev R, Shpirnaya I, Kasnak C, Palamutoglu R, Mardanshin I, Garipova S, Sobhani M, Aliniaeifard S (2020) The effect of endophytic bacteria Bacillus subtilis and salicylic acid on some resistance and quality traits of stored Solanum tuberosum L. tubers infected with fusarium dry rot. Plants 9(6):738. https://doi.org/10.3390/plants9060738
Li B, Li Q, Xu Z, Zhang N, Shen Q, Zhang R (2014) Responses of beneficial Bacillus amyloliquefaciens SQR9 to different soil-borne fungal pathogens through the alteration of antifungal compounds production. Front Microbiol 5:636
Mandal SD, Sonali, Singh S, Hussain K, Hussain T (2021) Plant Microbe Association for the mutual benefits for plant growth and soil health. In: Yadav AN et al (eds) Current Trends in microbial biotechnology for sustainable agriculture. Environmental and microbial biotechnology. Springer, Singapore, pp 95–121. https://doi.org/10.1007/978-981-15-6949-4_5
Mihajlović M, Rekanović E, Hrustić J, Grahovac M, Tanović B (2017) Methods for management of soil-borne plant pathogens. Pestic Fitomedicina 32:9–24
Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., p 433
Mnif I, Ghribi D (2016) Glycolipid biosurfactants: main properties and potential applications in agriculture and food industry. J Sci Food Agric 96(2):4310
Mohsin T, Sumera Y, Fauzia HY (2010) Biological control of Potato Black scurf by Rhizosphere associated Bacteria. Brazalian J Microbiol 41:439–451
Morikawa M, Hirata Y, Imanaka T (2000) A study on the structure-function relationship of lipopeptide biosurfactants. Biochim BiophysActa 1488:211–218
Morikawa M, Diado H, Takao T, Murata S, Shimonishi Y, Imanaka T (2003) A new lipopeptide biosurfactant produced by Arthrobacter sp. strain MIS38. J Bacterio 175:6459–6466
Mrabet M, Djebali N, ELKahoui S, Miloud Y, S. Saı¨di, B. Tarhouni, (2013) Efficacy of selected Pseudomonas strains for biocontrol of Rhizoctonia solani in potato. Phytopathol Mediterr 52:449–456
Muzhinji N, Woodhall JW, Truter M, van der Waals JE (2018) Variation in fungicide sensitivity among Rhizoctonia isolates recovered from potatoes in South Africa. Plant Dis 102(8):1520–1526
Nelson PE, Toussoun TA, Marassas WFO (1983) Fusarium species, an illustrated manual for identification, published by Pennsylvania State University: 135
Ogoshi A (1996) The genus Rhizoctonia. Rhizoctonia species: taxonomy, molecular biology, ecology, pathology and disease control. In: Sneh B, Jabaji-Hare S, Neate S, Dijst G (eds.). Kluwer Academic Publishers, Dordrecht: 1–9
Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125
Ongena M, Jacques P, Toure Y, Destain J, Jabrane A, Thonart P (2005) Involvement of fengycin-type lipopeptides in the multifaceted biocontrol potential of Bacillus subtilis. Appl Microbiol Biotechnol 69:29–38
Perneel M, Dhondt L, Maeyer De, KAdiobo A, Rabey K and Hofte M, (2008) Phenazines and biosurfactants interact in the biological control of soil-borne diseases caused by Phythium spp. Environmental Microb 10:778–788
Qiao X, Yu X, Liang Y, Liu R, Borriss R, Liu Y (2017) Addition of plant-growth-promoting Bacillus subtilis PTS-394 on tomato rhizosphere has no durable impact on the composition of root microbiome. BMC Microbiol 17(1):131–142
Reyes-ramírez A, Escudero-Abarca BI, Aguilar-Uscanga G, Hayward-Jones PM, Barboza-Corona JE (2006) Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J Food Sci 69:M131–M134
Said BH, Latifa S, Abdeljelil G, Abderrazak M (2012) Screening of potential biosurfactant producing bacteria isolated from seawater biofilm. Afri J Biotech 11(77):14153–14158
Saimmai A, Sobhon V, Maneerat S (2012) Production of biosurfactant from a new and promising strain of Leucobacter komagatae 183. Ann Microbiol 62:391–402
Sarwar A, Hassan MN, Imran M, Iqbal M, Majeed S, Brader G et al (2018a) Biocontrol activity of surfactin A purified from Bacillus NH-100 and NH-217 against rice bakanae disease. Microbiol Res 209:1–13
Sarwar A, Brader G, Corretto E, Aleti G, Abaidullah M, Sessitsch A et al (2018b) Qualitative analysis of biosurfactants from Bacillus species exhibiting antifungal activity. PLoS ONE 13(6):e0198107
Satpute SK, Bhawsar BD, Dhakephalkar PK, Chopade BA (2008) Assessment of different screening methods for selecting biosurfactant producing marine bacteria. Indian J Marine Sci 37:243–250
Shoeb E (2006) Genetic Basis of Heavy Metal Tolerance in Bacteria. Ph.D. thesis. University of Karachi, Karachi
Singh BP, Arora RK, Khurana SMP (2002) Soil and tuber borne diseases of potato. Central Potato Research Institute, Shimla, India. Technical Bulletin 41:74
Singh P, Hussain T, Patel S, Akhtar N (2018) Impact of climate change on root–pathogen interactions. In: Giri B, Prasad R, Varma A (eds) Root biology. Soil biology, vol 52. Springer, Cham. https://doi.org/10.1007/978-3-319-75910-4_16
Stefańczyk E, Sobkowiak S, Brylińska M et al (2016) Diversity of Fusarium spp. associated with dry rot of potato tubers in Poland. Eur J Plant Pathol 145:871–884. https://doi.org/10.1007/s10658-016-0875-0
Sundravadana S, Alice D, Kuttalam S, Samiyappan R (2007) Azoxystrobin activity on Rhizoctonia solani and its efficacy against rice sheath blight. Tunis J Plant Prot 2:79
Taheri P, Tarighi S (2010) Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway. J Plant Physiol 167:201–208
Tambekar DH, Gadakh PV (2013) Biochemical and molecular detection of biosurfactant producing bacteria from soil. Int J Life Sci Biotech Pharma Res 2(1):204–211
Tiwari RK, Kumar R, Sharma S et al (2020) Potato dry rot disease: current status, pathogenomics and management. 3 Biotech 10:503
Tomar S, Singh BP, Lal M, Khan MA, Hussain T, Sharma S, Kaushik SK, Kumar S (2014) Screening of novel microorganism for biosurfactant and biocontrol activity against Phytophthora infestans. J Environ Biol 35:893–899
Varadavenkatesan T, Murty VR (2013) Production and properties of a lipopeptide biosurfactant by B. subtilis subsp. inaquosorum. J Microbiol Biotechnol Res 3:63–73
Vater J, Gao X, Hitzeroth G, Wilde C, Franke P (2003) Whole cellºÐMatrix-assisted laser desorption ionization- time of flight mass spectrometry, an emerging technique for efficient screening of biocombinatorial libraries of natural compounds Present state of research. CCHTS 6:557–567
Vaux D, Cottingham M (2001) Method and apparatus for measuring surface configuration, patent number GB0001568.5
Velho RV, Medina LF, Segalin J, Brandelli A (2011) Production of lipopeptides among Bacillus strains showing growth inhibition of phytopathogenic fungi. Folia Microbiol (praha) 56:297–303
Virgen-Calleros G, Olalde-Portugal V, Carling DE (2000) Anastomosis groups of Rhizoctonia solani of potato in central Mexico and potential for biological and chemical control. Am J Potato Res 77:219–224
Wang X, Wang C, Li Q (2018) Isolation and characterization of antagonistic bacteria with the potential for biocontrol of soil-borne wheat diseases. J of Appl Microb 125(6):1868–1880
Windels CE, Brantner JR (2005) Early-season application of azoxystrobin to sugarbeet for control of Rhizoctonia solani AG 4 and AG 2–2. J Sugar Beet Res 42:1
Yan F, Xu S, Guo J, Chen Q, Meng Q, Zheng X (2015) Biocontrol of postharvest Alterneria alternate decay of cherry tomatoes with rhamnolipids and possible mechanism of action. J Sci Food Agric 95:1469–1474
Yoon SH et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617
Youssef NH, Duncan KE, Nagle DP, Savage KN, Knapp RM, McInerney MJJ (2004) Comparison of methods to detect biosurfactant production by diverse microorganisms. Microbiol Methods 56(3):339–347
Acknowledgements
The first author is highly thankful to SERB-Dept. of Science and Technology, New Delhi, Govt. of India, New Delhi, for providing the financial grants received under File No. DST-SERB-NPDF/2016/001409 and Dept. of Botany, Aligarh Muslim University, Aligarh, U.P for providing all the facilities/infrastructure, SAIF center for LC-MS-ESI, at CSIR-CDRI, Lucknow.
Funding
Science and Engineering Research Board, PDF/2016/001409, Touseef Hussain.
Author information
Authors and Affiliations
Contributions
TH: received the grant, conducted the study, write the draft, editing, AAK: guided and examine the findings.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hussain, T., Khan, A.A. Biocontrol prospective of Bacillus siamensis-AMU03 against Soil-borne fungal pathogens of potato tubers. Indian Phytopathology 75, 179–189 (2022). https://doi.org/10.1007/s42360-021-00447-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42360-021-00447-8