Bio efficacy of frog skin bacteria as biological control agents against chili anthracnose disease
Abstract
Amphibian skin e.g., frog carry bacterial symbionts on their skin that protect the frog from invasion of pathogen infection. This study aimed to evaluate antifungal activity of five bacterial skin frog (namely KSMD3; KSMD9; KSMD10; KSMV12; KSMV15) of Indonesian origin, Fejervarya limnocharis, against phytopathogen (Colletotrichum capsici) TCKr2. Primary screening for their antifungal activity was performed using dual culture method on nutrient agar contained 2% (w/v) of dextrose. The alteration of hyphal morphology on media and the detached chili fruit bioassay were observed. Isolate of KSMD3 was selected based on its significant performance in inhibiting the growth of the chili anthracnose pathogen, C. capsici. In addition, the KSMD3 showed low severity of disease incidence on detached chili fruit. Based on the analysis of 16S rDNA, the isolate of KSMD3 was identified as member of genera of Pseudomonas.
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References
Abbassi F, Oury B, Blasco T, Sereno D, Bolbach G, Nicolas P, Hani K, Amiche M, Ladram A. 2008. Isolation, characterization, and molecular cloning of new temporins from the skin of the North African ranid Pelophylax saharica. Peptides 29(9): 1526–1533.
Al-Ghaferi N, Kolodziejek J, Nowotny N, Coquet L, Jouenne T, Leprince J, Vaudry H, King, Jay. D, Conlon JM. 2010. Antimicrobial peptides from the skin secretions of the South-East Asian frog Hylarana erythraea (Ranidae). Peptides 31(4): 548–554.
Austin R. M. 2000. Cutaneous Microbial Flora and Antibiosis in Plethodon Ventralis. In: Bruce RG, Jaeger LD. Houck (eds) The Biology of Plethodontid Salamanders, 451–462): Springer US.
Cardoso JE, Santos AA, Rossetti AG, Vidal JC. 2004. Relationship between incidence and severity of cashew gummosis in semiarid north-eastern Brazil. Plant Pathology 53(3): 363–367.
Conlon JM. 2011. Clinical Applications of amphibian antimicrobial peptides. Journal of Medical Sciences, 4(2): 62–72. https://doi.org/10.2174/1996327001104020062.
D’Auria FD, Casciaro B, De Angelis M, Marcocci ME, Palamara AT, Nencioni L, Mangoni, ML. 2022. Antifungal activity of the frog skin peptide Temporin G and its effect on Candida albicans virulence factors. International Journal of Molecular Sciences 23(11): 6345.
Damasceno CL, Duarte EAA, dos Santos LBPR, de Oliveira TAS, de Jesus FN, de Oliveira LM, Góes-Neto A, Soares ACF. 2019. Postharvest biocontrol of anthracnose in bananas by endophytic and soil rhizosphere bacteria associated with sisal (Agave sisalana) in Brazil. Biological Control, 137, 104016.
Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD. 2012. The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens. Molecular Plant Pathology 13(4): 414–430.
De Silva DD, Crous PW, Ades PK, Hyde KD, Taylor PWJ. 2017. Lifestyles of Colletotrichum species and implications for plant biosecurity. Fungal Biology Reviews 31(3): 155–168.
Höfte M. 2021. The use of Pseudomonas spp. as bacterial biocontrol agents to control plant diseases. In: Wageningen University & Research, The Netherlands & J. Köhl (Eds.), Burleigh Dodds Series in Agricultural Science (pp. 301–374). Burleigh Dodds Science Publishing.
Iskandar DT, Erdelen WR. 2006. Conservation of amphibians and reptiles in Indonesia: Issues and problems 4(1): 60-87.
Jamalizadeh M, Etebarian HR, Aminian H, Alizadeh A. 2011. A review of mechanisms of action of biological control organisms against post-harvest fruit spoilage: A review of mechanisms of action of biological control organisms. EPPO Bulletin 41(1): 65–71.
Jared C, Mailho-Fontana PL, Marques-Porto R, Sciani JM, Pimenta DC, Brodie ED, Antoniazzi MM. 2018. Skin gland concentrations adapted to different evolutionary pressures in the head and posterior regions of the caecilian Siphonops annulatus. Scientific Reports 8(1): 3576.
Khan N, Maymon M, Hirsch A. 2017. Combating Fusarium infection using Bacillus-based antimicrobials. Microorganisms 5(4): 75.
Kim TJ, Sook-Young P, Woobong C, Yong-Hwan L, Heung TK. 2008. Characterization of Colletotrichum isolates causing anthracnose of pepper in Korea. Plant Pathology Journal 24(1): 17-23.
Köhl J, Kolnaar R, Ravensberg WJ. 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Frontiers in Plant Science 10: 845.
Kubota M, Abiko K. 2000. Induced resistance in hypocotyl of cucumber by infection with Colletotrichum lagenarium in leaves. J Gen Plant Pathol 66: 128–131.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547–1549.
Kwon HT, Lee Y, Kim J, Balaraju K, Kim HT, Jeon Y. 2022. Identification and characterization of Bacillus tequilensis GYUN-300: an antagonistic bacterium against red pepper anthracnose caused by Colletotrichum acutatum in Korea. Frontiers in Microbiology 13: 826827.
Lahlali R, Ezrari S, Radouane N, Kenfaoui J, Esmaeel Q, El Hamss H, Belabess Z, Barka EA. 2022. Biological control of plant pathogens: a global perspective. Microorganisms 10(3): 596.
Liu C, Hong J, Yang H, Wu J, Ma D, Li D, Lin D, Lai R. 2010. Frog skins keep redox homeostasis by antioxidant peptides with rapid radical scavenging ability. Free Radical Biology and Medicine 48(9): 1173–1181.
Liu F, Yang S, Xu F, Zhang Z, Lu Y, Zhang J, Wang G. 2022. Characteristics of biological control and mechanisms of Pseudomonas chlororaphis zm-1 against peanut stem rot. BMC Microbiology 22(1): 9 .
Madison JD, Berg EA, Abarca JG, Whitfield SM, Gorbatenko O, Pinto A, Kerby JL. 2017. Characterization of Batrachochytrium dendrobatidis Inhibiting bacteria from amphibian populations in Costa Rica. Frontiers in Microbiology 8: 290.
Mangoni ML, Miele R, Renda TG, Barra D, Simmaco M. 2001. The synthesis of antimicrobial peptides in the skin of Rana esculenta is stimulated by microorganisms. The FASEB Journal 15(8): 1431–1432.
McCoy KA, Peralta AL. 2018. Pesticides could alter amphibian skin microbiomes and the effects of Batrachochytrium dendrobatidis. Frontiers in Microbiology 9: 748.
Montri P, Taylor PWJ, Mongkolporn O. 2009. Pathotypes of Colletotrichum capsici, the causal agent of chili anthracnose in Thailand. Plant Disease 93(1): 17–20.
Saxena A, Raghuwanshi R, Gupta VK, Singh HB. 2016. Chilli anthracnose: the epidemiology and management. Frontiers in Microbiology 7: 1527.
Smith HK, Pasmans F, Dhaenens M, Deforce D, Bonte D, Verheyen K, Lens L, Martel A. 2018. Skin mucosome activity as an indicator of Batrachochytrium salamandrivorans susceptibility in salamanders. PLoS ONE 13(7): e0199295.
Stecher G, Tamura K, Kumar S. 2020. Molecular Evolutionary Genetics Analysis (MEGA) for macOS. Molecular Biology and Evolution 37(4): 1237–1239.
Susilawati L, Iwai N, Komatsu K, Arie T. 2021. Antifungal activity of bacteria isolated from Japanese frog skin against plant pathogenic fungi. Biological Control 153: 104498.
Than PP, Jeewon R, Hyde KD, Pongsupasamit S, Mongkolporn O, Taylor PWJ. 2008. Characterization and pathogenicity of Colletotrichum species associated with anthracnose on chilli (Capsicum spp.) in Thailand. Plant Pathology 57(3): 562–572.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acid. res. 22: 4673-4680.
Varga JFA, Bui-Marinos MP, Katzenback BA. 2019. Frog skin innate immune defences: sensing and surviving pathogens. Frontiers in Immunology 9: 3128.
Woodhams DC, LaBumbard BC, Barnhart KL, Becker MH, Bletz MC, Escobar LA, Flechas SV, Forman ME, Iannetta AA, Joyce MD, Rabemananjara F, Gratwicke B, Vences M, Minbiole KPC. 2018. Prodigiosin, violacein, and volatile organic compounds produced by widespread cutaneous bacteria of amphibians can inhibit two Batrachochytrium fungal pathogens. Microbial Ecology 75(4): 1049–1062.
Xu X, Lai R. 2015. The chemistry and biological activities of peptides from amphibian skin secretions. Chemical Reviews 115(4): 1760–1846.
Zepeda-Giraud LF, Olicón-Hernández DR, Pardo JP, Villanueva MGA, Guerra-Sánchez G. 2020. Biological control of Thielaviopsis paradoxa and Colletotrichum gloeosporioides by the extracellular enzymes of Wickerhamomyces anomalus. Agriculture 10(8): 325.
Al-Ghaferi N, Kolodziejek J, Nowotny N, Coquet L, Jouenne T, Leprince J, Vaudry H, King, Jay. D, Conlon JM. 2010. Antimicrobial peptides from the skin secretions of the South-East Asian frog Hylarana erythraea (Ranidae). Peptides 31(4): 548–554.
Austin R. M. 2000. Cutaneous Microbial Flora and Antibiosis in Plethodon Ventralis. In: Bruce RG, Jaeger LD. Houck (eds) The Biology of Plethodontid Salamanders, 451–462): Springer US.
Cardoso JE, Santos AA, Rossetti AG, Vidal JC. 2004. Relationship between incidence and severity of cashew gummosis in semiarid north-eastern Brazil. Plant Pathology 53(3): 363–367.
Conlon JM. 2011. Clinical Applications of amphibian antimicrobial peptides. Journal of Medical Sciences, 4(2): 62–72. https://doi.org/10.2174/1996327001104020062.
D’Auria FD, Casciaro B, De Angelis M, Marcocci ME, Palamara AT, Nencioni L, Mangoni, ML. 2022. Antifungal activity of the frog skin peptide Temporin G and its effect on Candida albicans virulence factors. International Journal of Molecular Sciences 23(11): 6345.
Damasceno CL, Duarte EAA, dos Santos LBPR, de Oliveira TAS, de Jesus FN, de Oliveira LM, Góes-Neto A, Soares ACF. 2019. Postharvest biocontrol of anthracnose in bananas by endophytic and soil rhizosphere bacteria associated with sisal (Agave sisalana) in Brazil. Biological Control, 137, 104016.
Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD. 2012. The Top 10 fungal pathogens in molecular plant pathology: Top 10 fungal pathogens. Molecular Plant Pathology 13(4): 414–430.
De Silva DD, Crous PW, Ades PK, Hyde KD, Taylor PWJ. 2017. Lifestyles of Colletotrichum species and implications for plant biosecurity. Fungal Biology Reviews 31(3): 155–168.
Höfte M. 2021. The use of Pseudomonas spp. as bacterial biocontrol agents to control plant diseases. In: Wageningen University & Research, The Netherlands & J. Köhl (Eds.), Burleigh Dodds Series in Agricultural Science (pp. 301–374). Burleigh Dodds Science Publishing.
Iskandar DT, Erdelen WR. 2006. Conservation of amphibians and reptiles in Indonesia: Issues and problems 4(1): 60-87.
Jamalizadeh M, Etebarian HR, Aminian H, Alizadeh A. 2011. A review of mechanisms of action of biological control organisms against post-harvest fruit spoilage: A review of mechanisms of action of biological control organisms. EPPO Bulletin 41(1): 65–71.
Jared C, Mailho-Fontana PL, Marques-Porto R, Sciani JM, Pimenta DC, Brodie ED, Antoniazzi MM. 2018. Skin gland concentrations adapted to different evolutionary pressures in the head and posterior regions of the caecilian Siphonops annulatus. Scientific Reports 8(1): 3576.
Khan N, Maymon M, Hirsch A. 2017. Combating Fusarium infection using Bacillus-based antimicrobials. Microorganisms 5(4): 75.
Kim TJ, Sook-Young P, Woobong C, Yong-Hwan L, Heung TK. 2008. Characterization of Colletotrichum isolates causing anthracnose of pepper in Korea. Plant Pathology Journal 24(1): 17-23.
Köhl J, Kolnaar R, Ravensberg WJ. 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Frontiers in Plant Science 10: 845.
Kubota M, Abiko K. 2000. Induced resistance in hypocotyl of cucumber by infection with Colletotrichum lagenarium in leaves. J Gen Plant Pathol 66: 128–131.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547–1549.
Kwon HT, Lee Y, Kim J, Balaraju K, Kim HT, Jeon Y. 2022. Identification and characterization of Bacillus tequilensis GYUN-300: an antagonistic bacterium against red pepper anthracnose caused by Colletotrichum acutatum in Korea. Frontiers in Microbiology 13: 826827.
Lahlali R, Ezrari S, Radouane N, Kenfaoui J, Esmaeel Q, El Hamss H, Belabess Z, Barka EA. 2022. Biological control of plant pathogens: a global perspective. Microorganisms 10(3): 596.
Liu C, Hong J, Yang H, Wu J, Ma D, Li D, Lin D, Lai R. 2010. Frog skins keep redox homeostasis by antioxidant peptides with rapid radical scavenging ability. Free Radical Biology and Medicine 48(9): 1173–1181.
Liu F, Yang S, Xu F, Zhang Z, Lu Y, Zhang J, Wang G. 2022. Characteristics of biological control and mechanisms of Pseudomonas chlororaphis zm-1 against peanut stem rot. BMC Microbiology 22(1): 9 .
Madison JD, Berg EA, Abarca JG, Whitfield SM, Gorbatenko O, Pinto A, Kerby JL. 2017. Characterization of Batrachochytrium dendrobatidis Inhibiting bacteria from amphibian populations in Costa Rica. Frontiers in Microbiology 8: 290.
Mangoni ML, Miele R, Renda TG, Barra D, Simmaco M. 2001. The synthesis of antimicrobial peptides in the skin of Rana esculenta is stimulated by microorganisms. The FASEB Journal 15(8): 1431–1432.
McCoy KA, Peralta AL. 2018. Pesticides could alter amphibian skin microbiomes and the effects of Batrachochytrium dendrobatidis. Frontiers in Microbiology 9: 748.
Montri P, Taylor PWJ, Mongkolporn O. 2009. Pathotypes of Colletotrichum capsici, the causal agent of chili anthracnose in Thailand. Plant Disease 93(1): 17–20.
Saxena A, Raghuwanshi R, Gupta VK, Singh HB. 2016. Chilli anthracnose: the epidemiology and management. Frontiers in Microbiology 7: 1527.
Smith HK, Pasmans F, Dhaenens M, Deforce D, Bonte D, Verheyen K, Lens L, Martel A. 2018. Skin mucosome activity as an indicator of Batrachochytrium salamandrivorans susceptibility in salamanders. PLoS ONE 13(7): e0199295.
Stecher G, Tamura K, Kumar S. 2020. Molecular Evolutionary Genetics Analysis (MEGA) for macOS. Molecular Biology and Evolution 37(4): 1237–1239.
Susilawati L, Iwai N, Komatsu K, Arie T. 2021. Antifungal activity of bacteria isolated from Japanese frog skin against plant pathogenic fungi. Biological Control 153: 104498.
Than PP, Jeewon R, Hyde KD, Pongsupasamit S, Mongkolporn O, Taylor PWJ. 2008. Characterization and pathogenicity of Colletotrichum species associated with anthracnose on chilli (Capsicum spp.) in Thailand. Plant Pathology 57(3): 562–572.
Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acid. res. 22: 4673-4680.
Varga JFA, Bui-Marinos MP, Katzenback BA. 2019. Frog skin innate immune defences: sensing and surviving pathogens. Frontiers in Immunology 9: 3128.
Woodhams DC, LaBumbard BC, Barnhart KL, Becker MH, Bletz MC, Escobar LA, Flechas SV, Forman ME, Iannetta AA, Joyce MD, Rabemananjara F, Gratwicke B, Vences M, Minbiole KPC. 2018. Prodigiosin, violacein, and volatile organic compounds produced by widespread cutaneous bacteria of amphibians can inhibit two Batrachochytrium fungal pathogens. Microbial Ecology 75(4): 1049–1062.
Xu X, Lai R. 2015. The chemistry and biological activities of peptides from amphibian skin secretions. Chemical Reviews 115(4): 1760–1846.
Zepeda-Giraud LF, Olicón-Hernández DR, Pardo JP, Villanueva MGA, Guerra-Sánchez G. 2020. Biological control of Thielaviopsis paradoxa and Colletotrichum gloeosporioides by the extracellular enzymes of Wickerhamomyces anomalus. Agriculture 10(8): 325.
Published
2023-06-21
How to Cite
SUSILAWATI, Lela et al.
Bio efficacy of frog skin bacteria as biological control agents against chili anthracnose disease.
Jurnal Biologi Udayana, [S.l.], v. 27, n. 1, p. 109-117, june 2023.
ISSN 2599-2856.
Available at: <https://ojs.unud.ac.id/index.php/bio/article/view/99034>. Date accessed: 21 nov. 2024.
doi: https://doi.org/10.24843/JBIOUNUD.2023.v27.i01.p11.
Section
Articles
