Abstract
Synthetic nematicides play an important role in the limitation of Meloidogyne incognita on agricultural fields. However, the reliance on synthetic nematicides has made them a threat to the environment due to their toxic nature. Application of rhizobacteria could reduce excessive dependency on their use. In view of the foregoing, an attempt was made to isolate and characterize growth-promoting bacterial strains through morphological and molecular methods. The 16 S rRNA gene sequencing exhibited identity with Streptomyces pseudogriseolus NRRL B-3288, Actinomyces hongkongensis H_KU8, Actinomyces liubingyangii VUL4_1, Pseudomonas amygdali AL1, Pseudomonas aeruginosa DSM 50,071 and Pseudomonas otitidis MCC10330. The growth-promoting ability of the isolated organisms was evaluated in sandy-loam, silty-loam and clay-loam soils planted with carrots in the screenhouse. This was compared with sole carbofuran and soil devoid of treatment. Their potency on M. incognita population was accessed simultaneously with the vegetative growth of carrot plants for 120 days. A probable degradation activity of the included organisms was also appraised. On the field, the organisms were assessed individually in sandy-loam soil. In the screenhouse, the organisms acted differently in disparate soils on their impact on M. incognita population and vegetative growth of carrot plants. Significant (p < 0.05) increase in vegetative growth and yield of carrot plants was noticed with inclusion of Actinomyces sp., in all soil classes. Pseudomonas sp., was not as effective as Actinomycetes sp., with regards to M. incognita population management and increase in yield. Nonetheless, Pseudomonas amygdali in sandy-loam soil exhibited a remarkable action on M. incognita population contrary to carbofuran alone. Secondly, on the field Actinomycetes sp., notably controlled M. incognita population and a remarkable reduction of egg mass and root galls was realized with an increase in yield. Evaluation of probable degradation of carbofuran with HPLC analysis revealed the presence of metabolites such as 3-hydroxy-carbofuran, 3-keto-carbofuran and carbofuran-phenol which implies that there was considerable degradation by the organisms. The growth-promoting attributes and nematicidal potential of S. pseudogriseolus, A. hongkongensis, A. liubingyangii, and P. amygdali have been established. These organisms are regarded as an excellent option in the management of M. incognita and they could be employed as part of the soil regimen in carrot production to reduce environmental contamination of synthetic nematicides.
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References
Abiodun OA, Dauda AO, Fabiyi OA, Akintayo FM (2022) Bio-fortification: quality improvement of Faba beans. In Faba Beans: Chemistry, Properties and Functionality. S.P. Bangar and S.B. Dhull (Eds). 275-300pp. DOI: https://doi.org/10.1007/978-3-031-14587-2_11
Amaresan N, Jayakumar V, Kumar K, Nooruddin T (2012) Isolation and characterization of plant growth promoting endophytic bacteria and their effect on tomato (Lycopersicon esculentum) and chilli (Capsicum annuum) seedling growth. Ann Microbiol 62:805–810
Atolani O, Fabiyi OA (2020) Plant Parasitic Nematodes Management Through Natural Products: Current Progress and Challenges. In Management of Phytonematodes: Recent Advances and Future Challenges. Ansari, R. A., Rizvi, R. and Mahmood, I. (Eds). 297–315. Singapore
Atolani O, Fabiyi OA, Olatunji GA (2014a) Isovitexin from Kigelia pinnata, a potential eco-friendly nematicidal agent. Trop Agric 19(2):67–74
Atolani O, Fabiyi OA, Olatunji GA (2014b) Nematicidal Isochromane Glycoside from Kigelia pinnata leaves. Acta Agriculturae Slovenica 104(1):25–31
Balakrishnan N, Gurusamy A, Nagarajan P (2013) An efficacious degradation of pesticide by salt tolerant Streptomyces venezuelae ACT 1. Bioresour Technol 132:378–382
Bello TT, Fabiyi OA, Clavero-Camacho I, Cantalapiedra-Navarrete C, Palomares-Rius JE, Castillo P, Archidona-Yuste A (2022) First report of Xiphinema ifacolum luc, 1961 (Dorylaimida: Longidoridae) from Nigeria. J Nematology 54:1–5. https://doi.org/10.2478/jofnem-2022-0015
Bremmer JM, Mulvaney CS (1982) Nitrogen-total. In: Page A.L., Miller R.H., Keeney D.R. (Ed) Methods of soil analysis, chemical and microbiological properties, Part 2, 2nd edition. ASA-SSSA, Madison, WI, pp 595–624
Briceño G, Fuentes MS, Saez MJ, Diez MC, Benimeli CS (2018) Streptomyces genus as biotechnological tool for pesticide degradation in polluted systems. Crit Rev Environ Sci Technol 48(10–12):773–805
Chapalmadugu S, Chaudhry GR. (1993) Isolation of a constitutively expressed enzyme for hydrolysis of carbaryl in Pseudomonas aeruginosa. Journal of Bacteriology. Oct;175(20):6711–6716. https://doi.org/10.1128/jb.175.20.6711-6716.1993. PMID: 8407847; PMCID: PMC206784
Chattopadhyay SK, Nandi B (1982) Inhibition of Helminthosporium oryzae and Alternariasolani by Streptomyces longisporus (Krasil’nokov) Waksman. Plant Soil 69:171–175
Chaudhry GR, Mateen A, Kaskar B, Bloda M, Riazuddin S (2002) Purification and characterization of the carbamate hydrolase from Pseudomonas sp. 50432. Appl Biochem Biotechnol 36:63–70
Chubachi K, Furakawa M, Fukuda S, Takahashi S, Matsumura S, Itagawa H, Shimizu T, Nakagawa A (1999) Control of root-knot nematodes by Streptomyces: screening of root-knot nematode controlling actinomycetes and evaluation of their usefulness in a pot test. Japanese J Nematology 29(2):42–45
Das K, Mukherjee AK (2006) Crude petroleum-oil biodegradation efficiency of Bacillus subtilis and Pseudomonas aeruginosa strains isolated from a petroleum-oil contaminated soil from North-East India. Bio-resource Technol 98(7):1339–1345
Dicklow MB, Acosta N, Zuckerman BM (1993) A novel Streptomyces species for controlling plant-parasitic nematodes. J Chem Ecol 19:159–173
Digrak M, Ozcelik S, Celik S (1995) Degradation of ethion and malathion by some microorganisms. 35th IUPAC Congress. Istanbul 14:19–84
Fabiyi OA (2019) Management of Groundnut (Arachis hypogea) Root-knot nematode (Meloidogyne incognita): Effect of Prosopis africana Pods. Indian J Nematology 49(2):214–216
Fabiyi OA (2020) Growth and yield response of groundnut Arachis hypogaea (Linn.) Under Meloidogyne incognita infection to furfural synthesised from agro-cellulosic materials. J Trop Agric 58(2):241–245
Fabiyi OA (2021a) Sustainable management of Meloidogyne incognita Infecting Carrot: Green synthesis of silver nanoparticles with Cnidoscolus aconitifolius: (Daucus carota). Vegetos 34(2):277–285
Fabiyi OA (2021b) Evaluation of plant materials as root-knot nematode (Meloidogyne incognita) suppressant in okro (Abelmuscous esculentus). Agriculturae Conspectus Scientificus 86(1):51–56
Fabiyi OA (2022a) Fractions from Mangifera indica as an alternative in Meloidogyne incognita Management. Pakistan J Nematology 40(1):65–74
Fabiyi OA (2022b) Cytotoxicity and nematicidal potential of Leaf extracts of Adansonia digitata and Khaya senegalensis on Root Knot Nematode (Meloidogyne incognita) Associated with Cabbage (Brassica oleracea). J Agricultural Sciences-Sri Lanka 17(3):425–436
Fabiyi OA (2022c) Evaluation of weeds against root-knot nematode (Meloidogyne incognita) in vegetables. Sarhad J Agric 38(4):1289–1299
Fabiyi OA (2022d) Application of composited municipal refuse dump site soil, orange, potato and pineapple peels in the control of root knot nematode (Meloidogyne incognita) infecting carrots (Daucus carota L). J Solid Waste Manage 48(3):474–485
Fabiyi OA, Alabi RO, Ansari RA (2020c) Nanoparticles’ Synthesis and Their Application in the Management of Phytonematodes: An Overview. In Management of Phytonematodes: Recent Advances and Future Challenges. Ansari, R. A., Rizvi, R. and Mahmood, I. (Eds). 125-140p. Singapore
Fabiyi OA, Atolani O, Olatunji GA (2020a) Toxicity Effect of Eucalyptus globulus on Pratylenchus spp of Zea mays Sarhad Journal of Agriculture. 36(4): 1244–1253
Fabiyi OA, Baker MA, Olatunji GA (2022) Application of fatty acid esters on Meloidogyne incognita infected Jew’s mallow. Pakistan J Nematology 40(2):127–137
Fabiyi OA, Claudius-Cole AO, Olatunji GA (2021b) In vitro assessment of n-phenyl imides in the management of Meloidogyne incognita. Scientia Agriculturae Bohemica 52(3):60–65
Fabiyi OA, Claudius-Cole AO, Olatunji GA, Abubakar DO, Adejumo OA (2021a) Evaluation of the in vitro response of Meloidogyne incognita to silver nano particle liquid from agricultural wastes. Agrivita J Agricultural Sci 43(3):524–534
Fabiyi OA, Olatunji GA (2021a) Environmental sustainability: Bioactivity of Leucaena leucocephala Leaves and Pesticide Residue analysis in Tomato Fruits. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 69(4):473–480
Fabiyi OA, Olatunji GA (2021b) Toxicity of derivatized citrulline and extracts of water melon rind (Citrullus lanatus) on root-knot nematode (Meloidogyne incognita). Trop Agric 98(4):347–355
Fabiyi OA, Olatunji GA, Daodu IO (2019) Nematicidal effect of organic extract metal c omplex on Meloidogyne incognita infecting groundnuts (Arachis hypogea). Scientia Agriculturae Bohemica 50(3):191–196
Fabiyi OA, Osunlola OS, Olatunji GA, Umar KA (2018) Efficacy of Agricultural Wastes in the control of Rice Cyst Nematode (Heterodera sacchari). Agriculturae Conspectus Scientificus 83(4):329–334
Fabiyi OA, Saliu OD, Claudius-Cole AO, Olaniyi IO, Oguntebi OV, Olatunji GA (2020b) Porous Starch Citrate Biopolymer for Controlled Release of Carbofuran in the Management of Root Knot Nematode Meloidogyne incognita Biotechnology Reports. 25:1–9 Published by Elsevier. https://doi.org/10.1016/j.btre.2020.e00428
Fareed A, Zaffar H, Rashid A, Naqvi TA (2017) Biodegradation of N methylated carbamates by free and immobilized cells of newly isolated strain Enterobacter cloacae strain TA7. Bioremediat J 21(3–4):119–127
Fenner K, Canonica S, Wackett LP, Elsner ME (2013) Evaluating pesticide degradation in the environment: Blind Spots and Emerging Opportunities. Science 341:752–758
Fuentes MS, Sineli PE, Pons S, Moreno de LeBlanc A, Benimeli CS, Hill RT, Cuozzo SA (2018) Study of the removal of a pesticides mixture by a Streptomyces strain and their effect on the cytotoxicity of treated systems. J Environ Chem Eng 6(6):6836–6843
Goad RT, Goad JT, Atieh BH, Gupta RC (2004) Carbofuran-induced endocrine disruption in adult male rats. Toxicol Mech Methods 14(4):233–239
Gopalakrishnan S, Srinivas V, Vidya MS, Rathore A (2013) Plant growth- promoting activities of Streptomyces spp. in sorghum and rice. Springer Plus 2:574–581
Hussain S, Ghaffar A, Aslam M (1990) Biological control of Macrophomina phaseolina charcoal rot of sunflower and mung bean. J Phytopathol 130:157–160
Ibitoye AA (2005) Laboratory Manual of Basic Methods in Analytical Chemistry. 1st Edition, Concept + IT and Educational Consult, Akure. Scientific Research. An academic Publisher, p 37
Jayabarath J, Musfira SA, Giridhar R, Arulmurugan R (2010) Biodegradation of Carbofuran Pesticide by saline soil Actinomycetes. Int J Biotechnol Biochem 6:187–193
Khan AA, Walia SK (1991) Expression, localization, and functional analysis of polychlorinated biphenyl degradation genes cbpABCD of Pseudomonas putida. Appl Environ Microbiol 57:1325–1332
Kim IS Ji Young Ryu, Hor Gil Hur, Man Bock Gu, Sang Don Kim and Jae Han Shim. (2004). Sphingomonas sp. strain SB5 degrades carbofuran to a new metabolite by hydrolysis at the furanyl ring.J. Agric Food Chem.52(8):2309–14
Kumar S, Mukerji KG, Lai R (1996) Molecular aspects of Pesticide degradation by microorganisms. Crit Rev Microbiol 22(1):1–26. https://doi.org/10.3109/10408419609106454
Lahdenpera¨ ML, Simon E, Uoti J (1991) Mycostop- a novel biofungicide based on Streptomyces bacteria, In A. B. R. Beemster, G. J. Bollen, M. Gerlach, M. A. Ruissen, B. Schippers, and R. A. Tempel (ed.), Biotic interactions and soil-borne diseases; proceedings of the 1st Conference of the European Foundation for Plant Pathology. Elsevier, Amsterdam. 258-263pp
Lau TK, Chu W, Graham N (2007) Degradation of the endocrine disruptor carbofuran by UV, O3 and O3/UV”. Water science and technology. J Int Association Water Pollution Res 55(12):275–280
Law JW, Ser HL, Khan TM (2017) The potential of Streptomyces as biocontrol gents against the rice blast fungus, Magnaporthe oryzae (Pyricularia oryzae). Frontiers in Microbiology. doi:https://doi.org/10.3389/fmicb.2017.00003
Li JS, Qi H, Zhang SY (2020) Two new milbemycin derivatives from a genetically engineered strain Streptomyces bingchenggensis. J Asian Nat Prod Res 1–6. https://doi.org/10.1080/10286020.2020.1783656
Liu J, Tan L, Wang J, Wang Z, Ni H, Li L (2016) Complete biodegradation of chlorpyrifos by engineered Pseudomonas putida cells expressing surface-immobilized laccases. Chemosphere 157:200–207
Margesin R, Schinner F, Miteva V (2005) Manual for Soil Analysis-Monitoring and assessing Soil Bioremediation. Technology 7(9):917–924
Mishra S, Pang S, Zhang W, Lin Z, Bhatt P, Chen S (2021) Insights into the microbial degradation and biochemical mechanisms of carbamates.Chemosphere.279
Mulbry WW, Eaton RW (1991) Purification and characterization of the N-methylcarbamate hydrolase from Pseudomonas strain CRL-OK. Appl Environ Microbiol 57(12):3679–3682
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural water. Annals Chem Acta 27:31–36
Naqvi TA, Armughan A, Ahmed N, Ahmed S (2013) Biodegradation of carbamates by Pseudomonas aeruginosa. Minerva Biotechnol 25:207–211
Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Page, A. L., Miller, R.H., and Keeney, D.R. (eds): Methods of Soil Analysis: Chemical and Microbiological Properties. Part 2, 2nd edition. ASA-SSSA Madison, WI 539-579pp
Nicosia S, Carr N, Gonzales DA, Orr MK (1991) Off-field movement and dissipation of soil incorporated commercial rice fields. J Environ Qual 20:532–539
Okalebo JR, Gathua KW, Woomer PL, Africa SACRED (2002) Second Edn Nairobi:Moi University,128
Pandey R (2011) Nematicidal activities of natural lignans and derivatives from milky thistle against Meloidogyne incognita. Indian J Phytopathol 6(2):182–185
Patil H, Chaudhari B (2011) Agricultural implications of Actinomycetes. In: Kumar A (ed) Environment and biotechnology. Daya Publishing House, New Delhi, India
Poiras N (2013) The effect of plant extracts and exometabolites of Streptomycetes bacteria on the behaviour of root-knot nematodes (Meloidogyne spp.) and root-lesion nematodes (Pratylenchus spp.). In: M.Sc. Thesis. Faculty of Science, Ghent University, Belgium, pp. 40
Rana S, Mardarveran P, Gupta R, Wahid Z (2019) Role of microbes in degradation of Chemical pesticides. In: Kumar A, Sharma S (eds) Microbes and enzymes in Soil Health and Bioremediation. Microorganisms for sustainability, vol 16. Springer, Singapore, pp 255–275. https://doi.org/10.1007/987-981-13-9117-0_11.
Rashad FM, Fathy HM, El-Zayat AS, Elghonaimy AM (2015) Isolation and characterization of multifunctional Streptomyces species with antimicrobial, nematicidal and phytohormone activities from marine environments in egyptian. J Microbiol Res 175:34–47
Rhoades JD (1982) Cation exchange capacity. In: Page AL, Miller RH, Keeney DR (eds) Ed) methods of soil analysis: chemical and microbiological properties. Part 2, 2nd edn. ASA-SSSA, Madison, pp 149–158
Rothrock CS, Gottlieb D (1984) Role of antibiosis in antagonism of Streptomyces hygroscopicus var geldanus to Rhizoctonia solani in soil. Can J Microbiol 30:1440–1447
Ruanpanun P, Chamswarng C (2016) Potential of Actinomycetes isolated from earthworm castings in controlling root-knot nematode: Meloidogyne incognita. J Gen Plant Pathol 82:43–50
Ruanpanun P, Dame ZT, Laatsch H (2011b) 3-Methoxy-2-methyl-carbazole-1, 4-quinone, carbazomycins D and F from Streptomyces sp. CMU-JT005. FEMS Microbiol Lett 322(1):77–81. https://doi.org/10.1111/j.1574-696802335.x
Ruanpanun P, Laatsch H, Tangchitsomkid N (2011a) Nematicidal activity of fervenulin isolated from a nematicidal actinomycete, Streptomyces sp. CMU-MH021, on Meloidogyne incognita. World J Microbiol Biotechnol 1(6):1373–1380. https://doi.org/10.1007/s11274-010-0588z
Saito A, Fujii T, Miyashita K (2003) Distribution and evolution of chitinase genes in Streptomyces species: involvement of gene duplication and domain-deletion. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology 84:7–16
Samac DA, Kindel LL (2001) Suppression of the root-lesion nematode (Pratylenchus penetrans) in alfalfa (Medicago sativa) by Streptomyces spp. Plant Soil 235:35–44
Saxena G (2004) Biocontrol of nematode-borne diseases in vegetable crops. Fruit and vegetable diseases 1:397–450. https://doi.org/10.1007/0-306-48575-3_11
Sharma JO (2019) Nematicidal potential of Streptomyces antibioticus strain M7 against Meloidogyne incognita. AMB Express 9(1):168. 10.118 6/s13568-019-0894-2
Simard RR (1993) Ammonium acetate-extractable elements. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis publishers, Boca Raton, F.L, pp 39–42
Smith S, Read D (1997) Mycorrhizal Symbiosis. Academic Press; London, UK: 1997. pp. 453–469
Subramani R, Sipkema D (2019) Marine rare actinomycetes: a promising source of structurally diverse and unique novel natural products. Mar Drugs 17(5):249
Sun, W., Xu, W., Zhang, W., Guang, C. and Mu.W. (2022). Microbial elimination of carbamate pesticides: specific strains and promising enzymes. Appl Microbiol Biotechnol. 106(18):5973–5986. https://doi.org/10.1007/s00253-022-12141-4.
Tanaka Y, Omura S (1993) Agroactive compounds of microbial origin. Annu Rev Microbiol 47:57–87
Tang YQ, Sattler I, Thiericke R, Grabley S, Feng XZ (2000) Parallel chromatography in natural products chemistry: isolation of new secondary metabolites from Streptomyces sp. In: Proceeding of the fourth international electronic conference on synthetic organic chemistry. http://www.mdpi.org/ecsoc-4.htm
Taylor AL, Sasser JN (1978) Identification and control of root-knot nematodes (Meloidogyne spp). Crop. Publ. Dept. Plant Pathol. North Carolina State Univ. and U.S Agency Int. Dev, Raleigh, N.C, p 111
Umuhoza, JNK, Sylvestre, H, Philippe, S (2014) Nutritional quality of carrot (Daucas carota L) as influenced by farm yard manure. World Journal of Agricultural Sciences 2(5):102–107
Viaene T, Langendries S, Beirinckx S, Maes M, Goormachtig S (2016)Streptomyces as plant’s best friend? FEMS Microbiology
Vurukonda S, Giovanardi D, Stefani E (2018) Plant growth promoting and Biocontrol Activity of Streptomyces sp. as endophytes. Int J Mol Sci 19(4):952. https://doi.org/10.3390/ijms19040952
Wadi JA, Easton GG (1985) Control of Verticillium dahliae by coating seed pieces with antagonistic bacteria. In: Parker CA, Rovira AD, Moore KJ, Wong PTW, Kollmorgen JF (eds) Ecology and management of soil-borne pathogens. American Phytopathology Society, St. Paul, Minn, pp 134–136
Yang LY, Wang JD, Zhang J, Xue CY, Zhang H, Wang XJ, Xiang WS (2013) New nemadectin congeners with acaricidal and nematocidal activity from Streptomyces microflavus neau 3 Y-3. Bioorg Med Chem Lett 23:5710–5713
Yin SY, Chang JK, Xun PC (1965) Studies in the mechanisms of antagonistic fertilizer ‘‘5406.’’ IV. The distribution of the antagonist in soil and its influence on the rhizosphere. Acta Microbiol Sinica 11:259–288
Yu CL, Tian J, Deng SQ, Zhao RX, Wang J, Chen LZ (2016) Study of the broad-spectrum pesticide degrading Actinomyces on the trichlorfon degradation characteristics. Genomics and Applied Biology 35(6):1451–1457.
Zeng Q, Huang H, Zhu J, Fang Z, Sun Q, Bao S (2013) A new nematicidal compound produced by Streptomyces albogriseolus HA10002. Antonie Van Leeuwenhoek 103:1107–1111
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Fabiyi, O.A., Adebisi, O.O., Falore, S.O. et al. Assessment of Actinomyces and Pseudomonas species on Meloidogyne incognita population and growth of carrot plants in disparate soils. Indian Phytopathology 76, 593–604 (2023). https://doi.org/10.1007/s42360-023-00629-6
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DOI: https://doi.org/10.1007/s42360-023-00629-6