Enhanced siderophore production by Pseudomonas aeruginosa and its antagonism against fungal threats in sesame fields

Authors

DOI:

https://doi.org/10.14719/pst.6148

Keywords:

antagonism, biocontrol, kerala, microbiology, PGPR, sustainable agriculture

Abstract

We succeeded in identifying and isolating three strains of Pseudomonas aeruginosa, namely, P2LA3, N3D3 and KMND3, from the soil of sesame (Sesamum indicum L.) cultivation fields in Onattukara, Alappuzha district, Kerala, India. Further in-depth microbiological studies reveal that the maximum siderophore yield is observed in strain KMND3 (70.9 µM), followed by P2LA3 (54 µM) and N3D3 (27 µM). All these strains showed considerable antagonism against significant sesame fungal pathogens such as Aspergillus flavus, Fusarium moniliforme, F. oxysporum and Rhizoctonia solani. Among these strains, KMND3 proved to be the most effective. Therefore, we focused on this strain for further study to demonstrate the influence of various physico-chemical parameters on siderophore production. This study identified several parameters that enhance production, such as starch as a carbon source, yeast as a nitrogen source and supplementary media containing Cd2+, Mn2+ and Hg2+. In contrast, a high concentration of iron was found to inhibit production. The results of our study confidently highlight the potential of P. aeruginosa strain KMND3 as a successful bio-control agent capable of suppressing fungal pathogens in sesame through siderophore-based mechanisms.

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References

Wei P, Zhao F, Wang Z, Wang Q, Chai X, Hou G, et al. Sesame (Sesamum indicum L.): A Comprehensive review of nutritional value, phytochemical composition, health benefits, development of food and industrial applications. Nutrients. 2022;14(19):4079.

FAOSTAT (Food and Agriculture Organization Statistical Databases) [internet]. FAOSTAT homepage [on-line]; 2019 [cited Nov 18 2024]. Available: http://faostat.fao.org.

Sharma VP. Oilseed production in India: the problems and prospects. New Delhi: Springer; 2017.

Official website of Intellectual Property India Geographical indication Registry [internet]; 2022 [cited 2022 Nov, 2024]. Available from: https://search.ipindia.gov.in/GIRPublic/Application/Details/736

None HHK, Jawaharlal NJ, Ranganatha, Chander S. Safe sesame (Sesamum indicum l.) production : perspectives, practices and challenges. J Oilseeds Res. 2015;30:32(1)1:24.

Ara A. Histopathological studies of sesame (Sesamum indicum) seedlings infected with Fusarium oxysporum. Plant Pathol Quar J Fungal Biol. 2017;7(1):82. https://doi.org/10.5943/ppq/7/1/10

Balakrishnan S, Sulochana KK. Fungal diseases of sesamum in Kerala. PhD [Thesis]. Vellayani: Department of Plant Pathology, College of Agriculture; 1989.

Klich MA. Aspergillus flavus: the major producer of aflatoxin. Mol Plant Pathol. 2007;8(6):713–22.

Ito K, Tanaka T, Hatta R, Yamamoto M, Akimitsu K, Tsuge T. Dissection of the host range of the fungal plant pathogen Alternaria alternata by modification of secondary metabolism. Mol Microbiol. 2004;19;52(2):399–411. https://doi.org/10.1111/j.1365-2958.2004.04004.x

Kumar K, Singh J, Saksena HK. Fungi associated with Sesamum seeds, their nature and control. Indian Phytopathol. 1984:37:330–32.

Jiao X, Takishita Y, Zhou G, Smith DL. Plant associated rhizobacteria for biocontrol and plant growth enhancement. Front Plant Sci. 2021;12:634796. https://doi.org/10.3389/fpls.2021.634796

Ren D, Zuo R, Wood TK. Quorum-sensing antagonist (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone influences siderophore biosynthesis in Pseudomonas putida and Pseudomonas aeruginosa. Appl Microbiol Biotechnol. 2004;66(6):689–95. https://doi.org/10.1007/s00253-004-1691-6

Berg G, Opelt K, Zachow C, Lottmann J, GÃtz M, Costa R, et al. The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol. 2006;56(2):250–61. https://doi.org/10.1111/j.1574-6941.2005.00025.x

Ghadamgahi F, Tarighi S, Taheri P, Saripella GV, Anzalone A, Kalyandurg PB, et al. Plant growth-promoting activity of Pseudomonas aeruginosa FG106 and its ability to act as a biocontrol agent against potato, tomato and taro pathogens. Biology (Basel). 2022;11(1):140. https://doi.org/10.3390/biology11010140

Rani R, Kumar V, Gupta P. Plant growth-promoting rhizobacteria-assisted bioremediation of toxic contaminant: recent advancements and applications. Elsevier eBooks; 2022. https://doi.org/10.1016/B978-0-323-85455-9.00003-5

Barbhaiya HB, Rao KK. Production of pyoverdine, the fluorescent pigment of Pseudomonas aeruginosa PAO1. FEMS Microbiol Lett. 1985;27(2):233–35.

Djibaoui D, Bensoltane A. Effect of iron and growth inhibitors on siderophores production by Pseudomonas fluorescens. Afr J Biotechnol. 2005;4(7):697–702. https://doi.org/10.5897/AJB2005.000-3129

El-Debaiky SA. Antagonistic studies and hyphal interactions of the new antagonist Aspergillus piperis against some phytopathogenic fungi in vitro in comparison with Trichoderma harzianum. Microb Pathog. 2017;113:135–43. https://doi.org/10.1016/j.micpath.2017.10.041

Patel PR, Shaikh SS, Sayyed RZ. Modified chrome azurol S method for detection and estimation of siderophores having affinity for metal ions other than iron. Environmental Sustainability. 2018;1(1):81–87. https://doi.org/10.1007/s42398-018-0005-3

Waday YA, Girma AE, Bultum MS, Ramayya AV, Beyene D. Isolation and characterization of plant growth-promoting rhizobacteria from coffee plantation soils and its influence on maize growth. Appl Environ Soil Sci. 2022;2022:e5115875. https://doi.org/10.1155/2022/511 5875

Cornu JY, Gutierrez M, Randriamamonjy S, Gaudin P, Ouedraogo F, Sourzac M, et al. Contrasting effects of siderophores pyoverdine and desferrioxamine B on the mobility of iron, aluminum and copper in Cu-contaminated soils. Geoderma. 2022;420:115897.

Vindeirinho JM, Helena, Soares EV. modulation of siderophore production by Pseudomonas fluorescens through the manipulation of the culture medium composition. Appl Biochem and Biotechnol. 2021;193(3):607–18. https://doi.org/10.1007/s12010-020-03349-z

Gu S, Yang T, Shao Z, Wang T, Cao K, Jousset A, et al. Siderophoremediated interactions determine the disease suppressiveness of microbial consortia. Collins CH, editor. mSystems. 2020;5(3). https://doi.org/10.1128/msystems.00811-19

Meyer JM, abdallah MA. The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. J Gen Microbiol. 1978;107(2):319–28. https://doi.org/10.1099/00221287-107-2-319

Johri BN, Rao CVS, Goel R. Fluorescent pseudomonads in plant disease management. In: Dadarwal KR, editor. Biotechnological approaches in soil microrganism for sustainable crop production. Jodhpur: Scientific Publishers; 1997. p. 193–221. https://doi.org/10.12691/wjar-6-4-2

Loper JE, Buyer JS. Siderophore in microbial interactions on plant surfaces. Mol Plant-Microbe Interact. 1991;4:5–13.

Chodat F, Gouda S. Contribution to the study of the pigment of Pseudomonas fluorescens Mig. Pathol Microbiol. 1961;24:840–47.

Pattan J, Swapnil K, Pattan S. I solation, production and optimization of siderophores (iron chilators) from Pseudomonas fluorescence NCIM 5096 and pseudomonas from soil rhizosphere and marine water. Int J Curr Microbiol App Sci. 2017;6(3):919–28. https://doi.org/10.20546/ijcmas.2017.603.109

Srikantappa NO, Somashekar AG, Malammanavar G, Krishnappa M. Seed-borne fungi of sesame (Sesamum indicum L.) seeds in Davanagere district and their effect on germination. Res Rev Biosci. 2009;3(4):157–63.

Mirsam H, Suriani, Kurniawati S, Purwanto OD, Muis A, Pakki S, et al. In vitro inhibition mechanism of Trichoderma asperellum isolates from corn against Rhizoctonia solani causing banded leaf and sheath blight disease and its role in improving the growth of corn seedlings. Egypt J Biol Pest Control. 2023;33(1). https://doi.org/10.1186/s41938-023-00729-5

Syed A. Antagonistic effects of some fluorescent pseudomonads strains against root-rot fungi (Rhizoctonia solani and Fusarium oxysporum) and root knot nematode (Meloidogyne incognita) on chili (Capsicum annum). World Appl Sci J. 2013 1 Jan;27(11). https://doi.org/10.5829/idosi.wasj.2013.27.11.825

Islam MdA, Nain Z, Alam MdK, Banu NA, Islam MdR. In vitro study of biocontrol potential of rhizospheric Pseudomonas aeruginosa against Fusarium oxysporum f. sp. cucumerinum. Egypt J Biol Pest Control. 2018;28(1). https://doi.org/10.1186/s41938-018-0097-1

Mahmoud S, El Farrag ES, Elymani A. Antifungal activity of pyocyanin produced by Pseudomonas aeruginosa against Fusarium oxysporum schlech a_root-rot_phytopathogenic_fungi. Int J PharmTech Res. 2016;9(8):4350.

Mishra J, Mishra I, Arora NK. 2,4-Diacetylphloroglucinol producing Pseudomonas fluorescens JM-1 for management of ear rot disease caused by Fusarium moniliforme in Zea mays L. 3 Biotech. 2022;12(6). https://doi.org/10.1007/s13205-022-03201-7

Showkat S. Biological control of Fusarium oxysporum and Aspergillus sp. By Pseudomonas fluorescens isolated from wheat rhizosphere soil of kashmir. IOSR J Pharm Biol Sci. 2012;1(4):24–32. https://doi.org/10.9790/3008-0142432

Nakkeeran S, Fernando WGD, Siddiqui ZA. Plant growth promoting rhizobacteria formulations and its scope in commercialization for the management of pests and diseases. In: Siddiqui ZA, editor. PGPR: biocontrol and biofertilization. Dordrecht: Springer. 2005;57–96 https://doi.org/10.1007/1-4020-4152-7

Manwar AV, Khandelwal SR, Chaudhari BL, Meyer JM, Chincholkar SB. Siderophore production by a marine Pseudomonas aeruginosa and its antagonistic action against phytopathogenic fungi. Appl Biochem Biotechnol. 2004;118(1-3):243–52. https://doi.org/10.1385/abab:118:1-3:243

Anjaiah V, Cornelis P, Koedam N. Effect of genotype and root colonization in biological control of Fusarium wilts in pigeonpea and chickpea by Pseudomonas aeruginosa PNA1. Can J Microbiol. 2003;49:85–91. https://doi.org/10.1139/w03-011

Buysens S, Heungens K, Poppe J, Hofte M. Involvement of pyochelin and pyoverdin in suppression of Pythium induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Appl Environ Microbiol. 1996;62:865–71. https://doi.org/10.1128/aem.62.3.865-871.1996

Bendale MS, Chaudhari B, Chincholkar SB. Influence of environmental factors on siderophore production by Streptomyces fulvissimus ATCC 27431. Current Trends in Biotech Pharm. 2009;3:362–71.

Sheng MM, Jia HK, Zhang GY, Zeng LN, Zhang TT, Long YH, et al. Siderophore production by rhizosphere biological control bacteria brevibacillus brevis gzdf3 of Pinellia ternata and its antifungal effects on Candida albicans. J Microbiol Biotechnol. 2020;30(5):689–99. https://doi.org/10.4014/jmb.1910.10066

Sasirekha B, Srividya S. Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chilli. Agric Nat Resour. 2016;50(4):250–56. https://doi.org/10.1016/j.anres.2016.

Das N, Vimala R, Karthika P. Biosorption of heavy metals-An overview. 2008;7(2):159–69.

Trindade IB, Paquete CM, Louro RO. 8 Extracellular redox chemistry. De Gruyter eBooks. 2021. https://doi.org/10.1515/9783110589771-014

Shi P, Xing Z, Zhang Y, Chai T. Effect of heavy-metal on synthesis of siderophores by Pseudomonas aeruginosa ZGKD3. Earth Environ Sci. 2017;52:012103–13. https://doi.org/10.1088/1742-6596/52/1/012103

Chang JS, Law R, Chang CC . Biosorption of lead, copper and cadmium by biomass of Pseudomonas aeruginosa PU21. Water Res. 1997;31:1651–58. https://doi.org/10.1016/S0043-1354(97)00008-0

Vraspir JM, Butler A. Chemistry of marine ligands and siderophores. Ann Rev Mar Sci. 2009;1(1):43–63. https://doi.org/10.1146/annurev.marine.010908.163712

Tailor AJ, Joshi BH, Bhakta CG, Gopal V. Characterization and optimization of siderophore production from Pseudomonas fluorescens strain isolated from sugarcane rhizosphere. J Environ Res Dev. 2012;6:688–94.

Srivastava P, Jaggi V, Dasila H, Sahgal M. Identification and characterization of siderophore positive pseudomonas from North indian rosewood (Dalbergia sissoo) roxb. Forest ecosystem. Int J Agric Sci Res . 2020;10:239–56.

Tank N, Rajendran N, Patel B, Saraf M. Evaluation and biochemical characterization of a distinctive pyoverdin from a pseudomonas isolated from chickpea rhizosphere. Braz J Microbiol. 2012;43(2):639–48. https://doi.org/10.1590/S1517-83822012000200028

Xiao R, Kisaalita WS. Purification of pyoverdines of Pseudomonas fluorescens 2-79 by copper-chelate chromatography. Appl Environ Microbiol. 1995;61(11):3769–74. https://doi.org/10.1128/aem.61.11.3769-3774.1995

Alain B, Gheysen I, Wathelet B, Henri M, Edmond de H. Highperformance liquid chromatography analyses of pyoverdin siderophores differentiate among phytopathogenic fluorescent Pseudomonas species. Appl Microbiology. 2003;69(2):1143–53. https://doi.org/10.1128/aem.69.2.1143-1153.2003

Published

20-02-2025 — Updated on 28-02-2025

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Karthika TP, Dileep C. Enhanced siderophore production by Pseudomonas aeruginosa and its antagonism against fungal threats in sesame fields. Plant Sci. Today [Internet]. 2025 Feb. 28 [cited 2025 Mar. 30];12(1). Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/6148

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