Growth inhibition of Fusarium solani and F. oxysporum by Streptomyces sasae TG01, and its ability to solubilize insoluble phosphate
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Abstract. Sudiana A, Putri A, Napitupulu TP, Purnaningsih I, Idris, Kanti A. 2020. Growth inhibition of Fusarium solani and F. oxysporum by Streptomyces sasae TG01, and its ability to solubilize insoluble phosphate. Biodiversitas 21: 429-435. Actinomycetes have been widely explored for new antibiotic production, but not many studies explore its abilities to inhibit the growth of phytopathogenic fungi and solubilize insoluble phosphate hence stimulate the growth of plants. We isolated Actinomycetes from the soil. Based on morphology, physiology, and 16S rDNA analyses, the isolate is closely related to Streptomyces sasae. The strain was able to inhibit the growth of phytopathogenic fungi Fusarium solani, and Fusarium oxysporum. S. sasae produced secondary metabolites 2-methyl-1,3-dioxolane as the major constituent. The strain assimilated variable carbon sources include L-arabinose, D-fructose, D-glucose, D-mannitol, Lactose, raffinose, L-rhamnose, and sucrose. The strain grew at pH 6.0 to 8.0, and at salinity (1-3%). Their growth was affected by the salinity level. The strain solubilized Ca-P at 1-3% salinity, but their ability to solubilize phosphate was influenced by salinity. The strain was also able to solubilize rock phosphate. Their ability to solubilize less soluble phosphate and inhibit the growth of F. solani and F. oxysporum may imply that this strain is potential for biocontrol agents. The 16S rRNA gene was submitted to DDBJ with the entry number 5df623c1a3c8820021322a36.TG01, and the accession number is LC514451.
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References
REFERENCES
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Atta HM. 2015. Biochemical studies on antibiotic production from Streptomyces sp .: Taxonomy, fermentation, isolation, and biological properties. J Saudi Chem Soc 19(1):12–22. DOI:10.1016/j.jscs.2011.12.011
Baharlouei A, Bonjar GHS. 2011. Biological control of Sclerotinia sclerotiorum (oilseed rape isolate) by an effective antagonist Streptomyces. Afr J Biotechnol 10(30): 5785–5794. DOI:10.5897/AJB10.2017
Basilio A, González I, Vicente MF, Gorrochategui J, Cabello A, González A, Genilloud O. 2003. Patterns of antimicrobial activities from soil actinomycetes isolated under different conditions of pH and salinity. J Appl Microbiol 2003;95:814-823. DOI:10.1046/j.1365-2672.2003.02049.x
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Chen Y, Zhou D, Qi D, Gao Z, Xie J. 2018. Growth promotion and disease suppression ability of a Streptomyces sp . CB-75 from banana rhizosphere soil. Front Microbiol 8(2704):1–18. DOI:10.3389/fmicb.2017.02704
Egamberdieva D, Botir H, Abeer H, Abd-Allah E F. 2014. Characterization of salt tolerant Enterobacter hormaechei strain associated with tomato root grown in arid saline soil. J Pure Appl Microbiol 8(5):4231–4239
El-naggar NE, El-bindary AA, Abdel-M, Nour NS. 2017. In vitro activity, extraction, separation and structure elucidation of antibiotic produced by Streptomyces anulatus NEAE-94 active against multidrug-resistant Staphylococcus aureus. Biotechnol Biotec Eq 31(2):418–430. DOI:10.1080/13102818.2016.1276412
Elad Y. 2000. Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot 19(8-10):709-714. DOI:10.1016/S0261-2194(00)00094-6
Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337(6098):1107-1111. DOI:10.1126/science.1220761
Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea JM. 2010. Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45(3):209–217. DOI:10.1016/j.apsoil.2010.04.007
Gopalakrishnan S., Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, … Rupela O. 2011. Evaluation of actinomycete isolates obtained from herbal vermicompost for the biological control of Fusarium wilt of chickpea. Crop Prot 30(8):1070–1078. DOI:10.1016/j.cropro.2011.03.006
Goudjal Y, Toumatia O, Yekkour A, Sabaou N, Mathieu F, Zitouni A. 2014. Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res 169(1):59-65. DOI:10.1016/j.micres.2013.06.014
Gul P, Bakht J. 2015. Antimicrobial activity of turmeric extract and its potential use in food industry. J Food Sci Tech 52(4):2272-2279. DOI:10.1007/s13197-013-1195-4
Heydari A, Pessarakli M. 2010. A review on biological control of fungal plant pathogens using microbial antagonists. J Biol Sci 10(4):273-290. DOI:10.3923/jbs.2010.273.290
Imai Y, Fujiwara T, Ochi K, Hosaka T. 2012. Development of the ability to produce secondary metabolites in Streptomyces through the acquisition of erythromycin resistance. J Antibiot 65(6):323–326. DOI:10.1038/ja.2012.16
Jacob S, Sajjalaguddam RR, Sudini HK. 2018. Streptomyces sp. RP1A-12 mediated control of peanut stem rot caused by Sclerotium rolfsii. J Integ Agr 17(4):892–900. DOI:10.1016/S2095-3119(17)61816-1
Wink MJ. 2016. Methods for the taxonomic description of the Actinobacteria, 1–42. https://doi.org/Retrieved from https://www.dsmz.de/bacterial-diversity/compendium-of-actinobacteria
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Keszler Á, Forgács E, Kótai L, Vizcaíno JA, Monte E, García-acha I. 2000. Separation and identification of volatile components in the fermentation broth of Trichoderma atroviride by solid-phase extraction and gas chromatography – mass spectrometry. J Chromatogr Sci 38:421–424.
Kim O, Cho Y, Lee K, Yoon S, Kim M, Na H, … Chun J. 2012 Introducing EzTaxon-e?: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62: 716–721. DOI:10.1099/ijs.0.038075-0
Kumar PS, Duraipandiyan V, Ignacimuthu S. 2014. Isolation, screening and partial purification of antimicrobial antibiotics from soil Streptomyces. Kaohsiung J Med Sci 30(9):435–446. DOI:10.1016/j.kjms.2014.05.006
Kumar RR, Jadeja VJ. 2016. Isolation of Actinomycetes: A Complete Approach. Int J Curr Microbiol Appl Sci 201;5(5):606-618. DOI:10.20546/ijcmas.2016.505.062
Lee H, Whang K. 2015. Streptomyces sasae sp . nov ., isolated from bamboo ( Sasa borealis ) rhizosphere soil. Int J Syst Evol Microbiol 65:3547–3551. DOI:10.1099/ijsem.0.000454
Nandhini U, Sangareshwari S, Lata K. 2015. Gas chromatograpy-mass spectrometry analysis of bioactive constituents from the marine Streptomyces. Asian J of Pharm Clin Res 8(2):6–8.
O’Brien PA. 2017. Biological control of plant diseases. Australas Plant Path 2017;46(4):293-304. DOI:10.1007/s13313-017-0481-4
Pandey A, Shukla A, Majumdar SK. 2005. Utilization of carbon and nitrogen sources by Streptomyces kanamyceticus M 27 for the production of an anti bacterial antibiotic. Afri J Biotechnol 4(9):909-910 http://www.academicjournals.org/AJB
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134 (3):1017-1026. DOI:10.1104/pp.103.026583
Sadeghi A, Soltani B M, Jouzani GS, Karimi E, Nekouei MK, Sadeghizadeh M. 2014. Taxonomic study of a salt tolerant Streptomyces sp. strain C-2012 and the effect of salt and ectoine on lon expression level. Microbiol Res 169(2-3):232-238. DOI:10.1016/j.micres.2013.06.010
Saravana KP, Duraipandiyan V, Ignacimuthu S. 2014. Isolation, screening and partial purification of antimicrobial antibiotics from soil Streptomyces sp. SCA 7. Kaohsiung J Med Sci 30(9):435–46. DOI:10.1016/j.kjms.2014.05.006
Sathya A, Vijayabharathi R, Gopalakrishnan S. 2017. Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7:102. DOI:10.1007/s13205-017-0736-3
Sengupta S, Pramanik A, Ghosh A, Bhattacharyya M. 2015. Antimicrobial activities of actinomycetes isolated from unexplored regions of Sundarbans mangrove ecosystem. BMC Microbiol 15(170). DOI:10.1186/s12866-015-0495-4
Shiva S, Prasad K, Giovanardi D, Stefani E. 2018. Plant growth promoting and biocontrol activity of Streptomyces spp . as endophytes. Int J Mol Sci 19: 1–26. DOI:/10.3390/ijms19040952
Srinivasan R, Yandigeri MS, Kashyap S, Alagawadi AR. 2012. Effect of salt on survival and P-solubilization potential of phosphate solubilizing microorganisms from salt affected soils. Saudi J Biol Sci 19(4):427-434. DOI:10.1016/j.sjbs.2012.05.004
Sudha S, Masilamani SM. 2012. Characterization of cytotoxic compound from marine sediment derived actinomycete Streptomyces avidinii strain SU4. Asian Pac J Trop Biomed 2(10):770–3. DOI:10.1016/S2221-1691(12)60227-5
Suwan N, Boonying W, Nalumpang S. 2012. Antifungal activity of soil actinomycetes to control chilli anthracnose caused by Colletotrichum gloeosporioides. J Agr Technol 8(2):725–737.
van der Meij A, Worsley SF, Hutchings MI, van Wezel GP. 2017. Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev 41(3):392-416. DOI:10.1093/femsre/fux005
Wang X, Xia K, Yang X, Tang C. 2019. Growth strategy of microbes on mixed carbon sources. Nature Commun 10:1279. DOI:10.1038/s41467-019-09261-3
Aouar L, Boulahrouf A. 2012. Taxonomic identification of rhizospheric actinobacteria isolated from Algerian semi-arid soil exhibiting antagonistic activities against plant fungal pathogens. Can J Plant Pathol 34(2):165–176. DOI:10.1080/07060661.2012.681396
Atta HM. 2015. Biochemical studies on antibiotic production from Streptomyces sp .: Taxonomy, fermentation, isolation, and biological properties. J Saudi Chem Soc 19(1):12–22. DOI:10.1016/j.jscs.2011.12.011
Baharlouei A, Bonjar GHS. 2011. Biological control of Sclerotinia sclerotiorum (oilseed rape isolate) by an effective antagonist Streptomyces. Afr J Biotechnol 10(30): 5785–5794. DOI:10.5897/AJB10.2017
Basilio A, González I, Vicente MF, Gorrochategui J, Cabello A, González A, Genilloud O. 2003. Patterns of antimicrobial activities from soil actinomycetes isolated under different conditions of pH and salinity. J Appl Microbiol 2003;95:814-823. DOI:10.1046/j.1365-2672.2003.02049.x
Blair JMA, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJV. 2015. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 13:2–51. DOI:10.1038/nrmicro3380
Chaudhary HS, Soni B, Shrivastava AR, Shrivastava S. 2017. Diversity and versatility of actinomycetes and its role in antibiotic production. J Appl Pharm Sci 3(8 Suppl 1):S83–S94. DOI:10.7324/JAPS.2013.38.S14
Chen Y, Zhou D, Qi D, Gao Z, Xie J. 2018. Growth promotion and disease suppression ability of a Streptomyces sp . CB-75 from banana rhizosphere soil. Front Microbiol 8(2704):1–18. DOI:10.3389/fmicb.2017.02704
Egamberdieva D, Botir H, Abeer H, Abd-Allah E F. 2014. Characterization of salt tolerant Enterobacter hormaechei strain associated with tomato root grown in arid saline soil. J Pure Appl Microbiol 8(5):4231–4239
El-naggar NE, El-bindary AA, Abdel-M, Nour NS. 2017. In vitro activity, extraction, separation and structure elucidation of antibiotic produced by Streptomyces anulatus NEAE-94 active against multidrug-resistant Staphylococcus aureus. Biotechnol Biotec Eq 31(2):418–430. DOI:10.1080/13102818.2016.1276412
Elad Y. 2000. Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Prot 19(8-10):709-714. DOI:10.1016/S0261-2194(00)00094-6
Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337(6098):1107-1111. DOI:10.1126/science.1220761
Franco-Correa M, Quintana A, Duque C, Suarez C, Rodríguez MX, Barea JM. 2010. Evaluation of actinomycete strains for key traits related with plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45(3):209–217. DOI:10.1016/j.apsoil.2010.04.007
Gopalakrishnan S., Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, … Rupela O. 2011. Evaluation of actinomycete isolates obtained from herbal vermicompost for the biological control of Fusarium wilt of chickpea. Crop Prot 30(8):1070–1078. DOI:10.1016/j.cropro.2011.03.006
Goudjal Y, Toumatia O, Yekkour A, Sabaou N, Mathieu F, Zitouni A. 2014. Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res 169(1):59-65. DOI:10.1016/j.micres.2013.06.014
Gul P, Bakht J. 2015. Antimicrobial activity of turmeric extract and its potential use in food industry. J Food Sci Tech 52(4):2272-2279. DOI:10.1007/s13197-013-1195-4
Heydari A, Pessarakli M. 2010. A review on biological control of fungal plant pathogens using microbial antagonists. J Biol Sci 10(4):273-290. DOI:10.3923/jbs.2010.273.290
Imai Y, Fujiwara T, Ochi K, Hosaka T. 2012. Development of the ability to produce secondary metabolites in Streptomyces through the acquisition of erythromycin resistance. J Antibiot 65(6):323–326. DOI:10.1038/ja.2012.16
Jacob S, Sajjalaguddam RR, Sudini HK. 2018. Streptomyces sp. RP1A-12 mediated control of peanut stem rot caused by Sclerotium rolfsii. J Integ Agr 17(4):892–900. DOI:10.1016/S2095-3119(17)61816-1
Wink MJ. 2016. Methods for the taxonomic description of the Actinobacteria, 1–42. https://doi.org/Retrieved from https://www.dsmz.de/bacterial-diversity/compendium-of-actinobacteria
Kadmiri IM, Chaouqui L, Azaroual SE, Sijilmassi B, Yaakoubi K, Wahby I. 2018. Phosphate-Solubilizing and Auxin-Producing Rhizobacteria Promote Plant Growth Under Saline Conditions. Arab J Sci Eng 43(7):3403-3415. DOI:10.1007/s13369-017-3042-9
Keszler Á, Forgács E, Kótai L, Vizcaíno JA, Monte E, García-acha I. 2000. Separation and identification of volatile components in the fermentation broth of Trichoderma atroviride by solid-phase extraction and gas chromatography – mass spectrometry. J Chromatogr Sci 38:421–424.
Kim O, Cho Y, Lee K, Yoon S, Kim M, Na H, … Chun J. 2012 Introducing EzTaxon-e?: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62: 716–721. DOI:10.1099/ijs.0.038075-0
Kumar PS, Duraipandiyan V, Ignacimuthu S. 2014. Isolation, screening and partial purification of antimicrobial antibiotics from soil Streptomyces. Kaohsiung J Med Sci 30(9):435–446. DOI:10.1016/j.kjms.2014.05.006
Kumar RR, Jadeja VJ. 2016. Isolation of Actinomycetes: A Complete Approach. Int J Curr Microbiol Appl Sci 201;5(5):606-618. DOI:10.20546/ijcmas.2016.505.062
Lee H, Whang K. 2015. Streptomyces sasae sp . nov ., isolated from bamboo ( Sasa borealis ) rhizosphere soil. Int J Syst Evol Microbiol 65:3547–3551. DOI:10.1099/ijsem.0.000454
Nandhini U, Sangareshwari S, Lata K. 2015. Gas chromatograpy-mass spectrometry analysis of bioactive constituents from the marine Streptomyces. Asian J of Pharm Clin Res 8(2):6–8.
O’Brien PA. 2017. Biological control of plant diseases. Australas Plant Path 2017;46(4):293-304. DOI:10.1007/s13313-017-0481-4
Pandey A, Shukla A, Majumdar SK. 2005. Utilization of carbon and nitrogen sources by Streptomyces kanamyceticus M 27 for the production of an anti bacterial antibiotic. Afri J Biotechnol 4(9):909-910 http://www.academicjournals.org/AJB
Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134 (3):1017-1026. DOI:10.1104/pp.103.026583
Sadeghi A, Soltani B M, Jouzani GS, Karimi E, Nekouei MK, Sadeghizadeh M. 2014. Taxonomic study of a salt tolerant Streptomyces sp. strain C-2012 and the effect of salt and ectoine on lon expression level. Microbiol Res 169(2-3):232-238. DOI:10.1016/j.micres.2013.06.010
Saravana KP, Duraipandiyan V, Ignacimuthu S. 2014. Isolation, screening and partial purification of antimicrobial antibiotics from soil Streptomyces sp. SCA 7. Kaohsiung J Med Sci 30(9):435–46. DOI:10.1016/j.kjms.2014.05.006
Sathya A, Vijayabharathi R, Gopalakrishnan S. 2017. Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7:102. DOI:10.1007/s13205-017-0736-3
Sengupta S, Pramanik A, Ghosh A, Bhattacharyya M. 2015. Antimicrobial activities of actinomycetes isolated from unexplored regions of Sundarbans mangrove ecosystem. BMC Microbiol 15(170). DOI:10.1186/s12866-015-0495-4
Shiva S, Prasad K, Giovanardi D, Stefani E. 2018. Plant growth promoting and biocontrol activity of Streptomyces spp . as endophytes. Int J Mol Sci 19: 1–26. DOI:/10.3390/ijms19040952
Srinivasan R, Yandigeri MS, Kashyap S, Alagawadi AR. 2012. Effect of salt on survival and P-solubilization potential of phosphate solubilizing microorganisms from salt affected soils. Saudi J Biol Sci 19(4):427-434. DOI:10.1016/j.sjbs.2012.05.004
Sudha S, Masilamani SM. 2012. Characterization of cytotoxic compound from marine sediment derived actinomycete Streptomyces avidinii strain SU4. Asian Pac J Trop Biomed 2(10):770–3. DOI:10.1016/S2221-1691(12)60227-5
Suwan N, Boonying W, Nalumpang S. 2012. Antifungal activity of soil actinomycetes to control chilli anthracnose caused by Colletotrichum gloeosporioides. J Agr Technol 8(2):725–737.
van der Meij A, Worsley SF, Hutchings MI, van Wezel GP. 2017. Chemical ecology of antibiotic production by actinomycetes. FEMS Microbiol Rev 41(3):392-416. DOI:10.1093/femsre/fux005
Wang X, Xia K, Yang X, Tang C. 2019. Growth strategy of microbes on mixed carbon sources. Nature Commun 10:1279. DOI:10.1038/s41467-019-09261-3
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