Antagonistic Ability and Fungicide Tolerance of Rhizosphere Actinomycetes from the Hungayono Karst Ecosystem, Gorontalo

Nazifah R Adam, Yuliana Retnowati, Abubakar Sidik Katili, Novri Youla Kandowangko, Wirnangsi D. Uno

Abstract


Actinomycetes show promise as biological control agents, reducing fungicide use in agriculture due to their bioactive compounds and ecological resilience. This study focused on the initial screening and ecological bioprospecting of actinomycetes from the Hungayono karst ecosystem in Gorontalo by determining their antagonistic activity against the pathogenic fungi Fusarium oxysporum and Neocosmospora solani, as well as their tolerance to the fungicides thiram and benomyl. Potential isolates were identified using molecular methods. Samples were collected from three locations. Rhizosphere soil samples were obtained from plant species: Alocasia macrorrhizos, Ficus microcarpa, and Acrostichum aureum L. Antagonistic activity against root-pathogenic fungi and tolerance to fungicides were used as initial screening criteria to assess their potential as biological control agents. This study successfully isolated 9 actinomycete isolates. The results showed that only 33% of the isolates exhibited inhibitory activity, with isolate RzAH-07 showing a moderate inhibition zone (5.22 mm) against Fusarium oxysporum and weak inhibition (4.18 mm) against Neocosmospora solani, while also demonstrating tolerance to the fungicide benomyl up to 1000 ppm. RzAH-07 was selected as the top candidate due to its two key advantages. Phylogenetic analysis based on 16S rRNA gene sequences indicates that RzAH-07 is closely related to the genus Streptomyces, with a similarity percentage ranging from 98.35% to 99.14% based on GenBank data.


Keywords


Biocontrol; Fungicide tolerance; Karst; Rhizosphere; Streptomyces

Full Text:

PDF

References


Al-Hatmi AMS, Meis JF, De Hoog GS. 2016. Fusarium: Molecular diversity and intrinsic drug resistance. PLoS Pathog 12(4), E1005464. DOI:10.1371/journal.ppat.1005464.

Ariandi MZT, Bahar M, Yusmaini H, Zulfa F, Fauziah C, Pramesyanti A. 2021. Effectiveness of metabolite substance filtrates of actinomycetes isolates from Kebun Raya Bogor against the growth of Escherichia coli, Pseudomonas aeruginosa and Salmonella typhi: In vitro study. J Biol Trop 21 (1): 281-287. DOI: 10.29303/jbt.v21i1.2466.

Babalola OO, Oyedoh OP, Ayangbenro AS. 2025. Draft genome sequence of Streptomyces sp. OP7 and Streptomyces harbinensis OP7 strains isolated from Zea mays and Helianthus annuus rhizosphere soil. Microbiol Resour Announc 14(7) 01110-24. DOI: 10.1128/mra.01110-24

Bai S, Zhang M, Tang S, Li M, Wu R, Wan S, Chen L, Wei X, Li F. 2024. Research progress on benzimidazole fungicides: A review. Molecules, 29(6), 1218. DOI:10.3390/molecules29061218.

Bataeva Y, Delegan Y, Bogun A, Shishkina L, Grigoryan L. 2024. Whole genome analysis and assessment of the metabolic potential of Streptomyces carpaticus SCPM-O-B-9993, a promising phytostimulant and antiviral agent. Biology 13 (6): 388. DOI: 10.3390/biology13060388

Campanale C, Triozzi M, Ragonese A, Losacco D, Massarelli C. 2023. Dithiocarbamates: Properties, methodological approaches and challenges to their control. Toxics, 11(10), 851. DOI:10.3390/toxics11100851.

De Simeis D, Serra S. 2021. Actinomycetes: A never-ending source of bioactive compounds—an overview on antibiotics production. Antibiotics 10(5). MDPI AG. DOI:10.3390/antibiotics10050483.

Dewi SCO, Suprayogo D, Rahmanto D, Rini TS. 2024. Optimalisasi dan uji efektivitas Actinomycetes pada Brassica chinensis di bawah cekaman kekeringan dan pH masam Ultisol. J Tanah dan Sumberdaya Lahan 11 (1): 193-204. DOI:10.21776/ub.jtsl.2024.011.1.21.

Edlinger A, Garland G, Hartman K, Banerjee S, Degrune F, Garcia-Palacios P, Hallin S, Valzano-Held A, Herzog C, Jansa J, Kost E, Maestre FT, Pescador DS, Philippot L, Rillig MC, Romdhane S, Saghai A, Spor A, Frossard E, Van Der Heijden MGA. 2022. Agricultural management and pesticide use reduce the functioning of beneficial plant symbionts. Nat Eco. Evol. 6 (8): 1145-1154. DOI:10.1038/s41559-022-01799-8.

Elshafie HS, Camele I. 2022. Rhizospheric actinomycetes revealed antifungal and plant-growth-promoting activities under controlled environment. Plants 11 (14): 1872. DOI:10.3390/plants11141872.

Ghoul M, Mitri S. 2016. The ecology and evolution of microbial competition. Trends Microbiology 24 (10): 833-845. DOI:10.1016/j.tim.2016.06.011.

Hong SH, Song YS, Seo DJ, Kim KY, Jung WJ. 2017. Antifungal activity and expression patterns of extracellular chitinase and ?-1,3-glucanase in Wickerhamomyces anomalus EG2 treated with chitin and glucan. Microb Pathog 110: 159-164. DOI:10.1016/j.micpath.2017.06.038.

Hossain N, Rahman M. 2014. Antagonistic activity of antibiotic-producing Streptomyces sp. against fish and human pathogenic bacteria. B Braz. Arch. Biol Technol 57 (2): 233-237. DOI:10.1590/S1516-89132014000200011.

Hugoni M, Luis P, Guyonnet J, Haichar FEZ. 2018. Plant host habitat and root exudates shape fungal diversity. Mycorrhiza 28 (5-6): 451-463. DOI:10.1007/s00572-018-0857-5.

Indra P, Dalimunthe R, Batara E, Siregar M, Anna N. 2015. Respon Cylindrocladium sp. terhadap fungisida berbahan aktif mancozeb secara in vitro. Peronema For Sci J 4: 104-114.

Katili AS, Retnowati Y. 2017. Short communication: Isolation of actinomycetes from mangrove ecosystem in Torosiaje, Gorontalo, Indonesia. Biodiversitas 18 (2): 826-833. DOI:10.13057/biodiv/d180256.

Lamichhane JR, Barbetti MJ, Chilvers MI, Pandey AK, Steinberg C. 2024. Exploiting root exudates to manage soil-borne disease complexes in a changing climate. Trends Microbiology 32 (1): 27-37. DOI:10.1016/j.tim.2023.07.011.

Lugtenberg B, Rozen DE, Kamilova F. 2017. Wars between microbes on roots and fruits. F1000Research 6: 343. DOI:10.12688/f1000research.10696.1.

Luo Y, Shi C, Yang S, Liu Y, Zhao S, Zhang C. 2023. Characteristics of soil calcium content distribution in karst dry-hot valley and its influencing factors. Water 15 (6): 1119. DOI:10.3390/w15061119.

Mahato S, Lamichhane GC, Thakur A. 2021. Isolation and screening of antibiotic producing actinomycetes from soils of hills and plains of Eastern Nepal. JSM Clin Pharm 5 (1): 1019. DOI: 10.47739/2379-9498/1019.

Matalauni CL, Retnowati Y, Katili AS, Hasan AM, Kandowangko NY. 2025. Isolation and characterization of actinomycetes from plant rhizosphere in Gorontalo karst area. Mikhayla: J Adv Res 2 (1): 11-18. DOI:10.61579/Mikhayla.V2i1.286.

Meena RS, Kumar S, Datta R, Lal R, Vijayakumar V, Brtnicky M, Sharma MP, Yadav GS, Jhariya MK, Jangir CK, Pathan SI, Dokulilova T, Pecina V, Marfo TD. 2020. Impact of agrochemicals on soil microbiota and management: A review. Land 9 (2): 34. DOI:10.3390/land9020034.

Meenakshi S, Hiremath J, Meenakshi MH, Shivaveerakumar S. 2024. Actinomycetes: Isolation, cultivation and its active biomolecules. J Pure Appl Microbiol 18 (1): 118-143. DOI:10.22207/JPAM.18.1.48.

Meliani H, Makhloufi A, Cherif A, Mahjoubi M, Makhloufi K. 2022. Biocontrol of toxinogenic Aspergillus flavus and Fusarium oxysporum f. sp. albedinis by two rare Saharan actinomycetes strains and LC-ESI/MS-MS profiling of their antimicrobial products. Saudi J Biol Sci 29 (6): 103288. DOI:10.1016/j.sjbs.2022.103288.

Mirghani R, Saba T, Khaliq H, Mitchell J, Do L, Chambi L, Diaz K, Kennedy T, Alkassab K, Huynh T, Elmi M, Martinez J, Sawan S, Rijal G. 2022. Biofilms: Formation, drug resistance and alternatives to conventional approaches. AIMS Microbiol 8 (3): 239-277. DOI:10.3934/microbiol.2022019.

Muslim A, Suwandi. 2023. Pengendalian Hayati Patogen Tanaman dengan Mikroorganisme Antagonis Edisi Revisi I. Unsri Press, Palembang. www.unsri.unsripress.ac.id.

Mordor Intelligence. 2026. Indonesia fungicide market size & share analysis growth trends and forecast (2026-2031). [online]. www.mordorintelligence.com/industry-reports/indonesia-fungicide-market. [23 April 2026].

Ngamcharungchit C, Chaimusik N, Panbangred W, Euanorasetr J, Intra B. 2023. Bioactive metabolites from terrestrial and marine actinomycetes. Molecules 28 (15): 5915. DOI:10.3390/molecules28155915.

Okolie PI, Opara CN, Emerenini EC. 2013. Evaluation of bacterial diversity in palm wine by 16S rDNA analysis of community DNA. Niger Food J 31 (1): 83-90. DOI:10.1016/S0189-7241(15)30060-6.

Pandey K, Saharan BS. 2025. Soil microbiomes: A promising strategy for boosting crop yield and advancing sustainable agriculture. Discov Agric 3 (1): 54. DOI:10.1007/s44279-025-00208-5.

Pathalam G, Rajendran HAD, Appadurai DR, Gandhi MR, Michael GP, Savarimuthu I, Naif AAD. 2017. Isolation and molecular characterization of actinomycetes with antimicrobial and mosquito larvicidal properties. Beni-Suef Univ J Basic Appl Sci 6 (2): 209-217. DOI:10.1016/j.bjbas.2017.04.002.

Praptiwi, Fathoni A, Putri AL, Wulansari D, Agusta A. 2023. Biological potency of actinomycetes extracts from rhizosphere soil of Dacrycarpus imbricatus from Toba Samosir, North Sumatra. J Appl Pharm Sci 13(06): 146-153. DOI: 10.7324/JAPS.2023.106853.

Priyadarshini C, Lal R, Yuan P, Liu W, Adhikari A, Bhandari S, Xia Y. 2025. Plant disease suppressiveness enhancement via soil health management. Biology 14 (8): 924. DOI:10.3390/biology14080924.

Retnowati Y, Kandowangko NY, Katili AS, Pembengo W. 2024. Diversity of actinomycetes on plant rhizosphere of karst ecosystem of Gorontalo, Indonesia. Biodiversitas 25 (3): 907-915. DOI:10.13057/Biodiv/D250301.

Retnowati Y, Katili AS. 2023. Antibacterial activity of sponge-associated bacteria from Torosiaje marine area, Gorontalo, Indonesia. Biodiversitas 24 (2). DOI:10.13057/biodiv/d240255.

Retnowati Y, Katili AS, Kandowangko NY. 2025. Bioprospecting and molecular identification of Streptomyces on karst ecosystems in the coastal area of Gorontalo, Indonesia, as plant growth-promoting rhizobacteria. Biodiversitas 26 (7): 3294-3301. DOI:10.13057/biodiv/d260721.

Retnowati Y, Katili AS, Kandowangko NY, Pembengo W. 2024. Molecular identification of rhizospheric actinomycetes from karst ecosystems of Gorontalo, Indonesia, and its seed germination induction capability of Zea mays var. Doti. Biodiversitas 25 (12): 4763-4771. DOI: 10.13057/biodiv/d251212.

Retnowati Y, Sembiring L, Moeljopawiro S, Djohan TS, Soetarto ES. 2017. Diversity of antibiotic-producing actinomycetes in mangrove forest of Torosiaje, Gorontalo, Indonesia. Biodiversitas 18 (4): 1453-1461. DOI:10.13057/biodiv/d18032.

Sari AL, Hasanuddin, Lubis L. 2021. The effectiveness of contact fungicides mancozeb in controlling potato leaf blight disease (Phytophthora infestans (Mont) de Barry) in Karo District in the wet month and in the laboratory. IOP Conf Ser: Earth Environ Sci 782 (4): 042022. DOI:10.1088/1755-1315/782/4/042022.

Schaeffer A, Wijntjes C. 2022. Changed degradation behavior of pesticides when present in mixtures. Eco-Environ Health 1 (1): 23-30. DOI:10.1016/J.Eehl.2022.02.002.

Shahrajabian MH, Sun W. 2025. Microbial interaction of actinobacteria strains with various plants, promote growth and development in natural farming, and alleviating biotic and abiotic stresses. Discov Sustain 6 (1): 564. DOI:10.1007/S43621-025-01413-4.

Shirokikh IG, Shirokikh AA. 2019. Antagonism and resistance to antibiotics of actinomycetes from soils of three specially protected natural territories. Eurasian Soil Sci 52 (10): 1227-1233. DOI:10.1134/S1064229319100132.

Solomon W, Janda T, Molnar Z. 2024. Unveiling the significance of rhizosphere: Implications for plant growth, stress response, and sustainable agriculture. Plant Physiol Biochem 206: 108290. DOI:10.1016/J.Plaphy.2023.108290.

Tolodo DD, Manyoe IN, Arifin YI. 2022. Geochemistry characteristics of the Hungayono geothermal area for the development of clean energy in Gorontalo Province. IOP Conf Ser: Earth Environ Sci 1089 (1): 012020. DOI:10.1088/1755-1315/1089/1/012020.

Wang Z, Yun S, An Y, Shu L, Li S, Sun K, Zhang W. 2025. Effect of fungicides on soil respiration, microbial community, and enzyme activity: A global meta-analysis (1975-2024). Ecotoxicol Environ Saf 289: 117433. DOI:10.1016/J.Ecoenv.2024.117433.

Yadav AN, Verma P, Kumar S, Kumar V, Kumar M, Kumari Sugitha TC, Singh BP, Saxena AK, Dhaliwal HS. 2018. Actinobacteria from rhizosphere. In: Yadav AN, Mishra S, Singh S, Gupta A (eds.). New Future Dev Microb Biotechnol Bioeng. Elsevier, Amsterdam (13-41). Elsevier. DOI:10.1016/B978-0-444-63994-3.00002-3.

Yan X, Li Y, Wang N, Chen Y, Huang LL. 2018. Streptomyces ginkgonis sp. nov., an endophyte from Ginkgo biloba. Antonie van Leeuwenhoek 111 (6): 891-896. DOI: 10.1007/s10482-017-0987-3

Yin Y, Miao J, Shao W, Liu X, Zhao Y, Ma Z. 2023. Fungicide resistance: Progress in understanding mechanism, monitoring, and management. Phytopathology 113 (4): 707-718. DOI:10.1094/PHYTO-10-22-0370-KD




DOI: https://doi.org/10.14421/biomedich.2026.151.895-905

Refbacks

  • There are currently no refbacks.




Copyright (c) 2026 Nazifah R Adam, Yuliana Retnowati, Abubakar Sidik Katili, Novri Youla Kandowangko, Wirnangsi D. Uno



Biology, Medicine, & Natural Product Chemistry
ISSN 2089-6514 (paper) - ISSN 2540-9328 (online)
Published by Sunan Kalijaga State Islamic University & Society for Indonesian Biodiversity.

CC BY NC
This work is licensed under a CC BY-NC