Skip to main content
SpringerLink
Log in

Exploring the Trends in Actinobacteria as Biological Control Agents of Phytopathogenic Fungi: A (Mini)-Review

  • REVIEW ARTICLE
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Biological control has been considered a sustainable alternative to combat phytopathogens. The increase of studies in the past few years involving Actinobacteria as biological control agents of phytopathogenic fungi has motivated us to search for which Actinobacteria genus that have been studied in the last five years and explore their mechanisms of antifungal activity. The accesses were carried out on three multidisciplinary digital platforms: PubMED/MedLine, Web of Science and Scopus. Actinobacteria from genus Amycolatopsis, Curtobacterium, Kocuria, Nocardioides, Nocardiopsis, Saccharopolyspora, Streptoverticillium and especially Streptomyces showed a broad antifungal spectrum through several antibiosis mechanisms such as the production of natural antifungal compounds, siderophores, extracellular hydrolytic enzymes and activation of plant defense system. We observed the formation of a methodology based on antagonistic compounds bioactivity to select efficient Actinobacteria to be used as biological control agents against phytopathogenic fungi. The use of multifunctional Actinobacteria has been proven to be efficient, not only by its natural protective activity against phytopathogenic fungi but also because of their ability to act as plant growth-promoting bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of Data and Materials

The data and material that support the findings of this study are openly available in PubMED/MedLine, Web of Science and Scopus at https://pubmed.ncbi.nlm.nih.gov/, https://clarivate.com/webofsciencegroup/ and https://www.scopus.com/, respectively.

References

  1. Ashfield-Crook NR, Woodward Z, Soust M, Kurtböke Dİ (2018) Assessment of the detrimental impact of polyvalent streptophages intended to be used as biological control agents on beneficial soil streptoflora. Curr Microbiol 75:1589–1601. https://doi.org/10.1007/s00284-018-1565-2

    Article  CAS  PubMed  Google Scholar 

  2. Patel JK, Madaan S, Archana G (2018) Antibiotic producing endophytic Streptomyces spp. colonize above-ground plant parts and promote shoot growth in multiple healthy and pathogen-challenged cereal crops. Microbiol Res 215:36–45. https://doi.org/10.1016/j.micres.2018.06.003

    Article  CAS  PubMed  Google Scholar 

  3. Andargie M, Li J (2019) Antifungal activity against plant pathogens by compounds from Streptoverticillium morookaense. J Plant Pathol 101:547–558. https://doi.org/10.1007/s42161-018-00234-x

    Article  Google Scholar 

  4. Kouomou PFD, Ewane CA, Lerat S, Ndoumou DO, Beaulieu C, Boudjeko T (2019) Evaluation of antagonistic activities against Pythium myriotylum and plant growth promoting traits of Streptomyces isolated from Cocoyam (Xanthosoma sagittifolium (L.) Schott) rhizosphere. Aust J Crop Sci 13:920–933. https://doi.org/10.21475/ajcs.19.13.06.p1670

    Article  CAS  Google Scholar 

  5. Xu W, Wang F, Zhang M, Ou T, Wang R, Strobel G et al (2019) Diversity of cultivable endophytic bacteria in mulberry and their potential for antimicrobial and plant growth-promoting activities. Microbiol Res 229:126328. https://doi.org/10.1016/j.micres.2019.126328

    Article  CAS  PubMed  Google Scholar 

  6. Sujarit K, Mori M, Dobashi K, Shiomi K, Pathom-Aree W, Lumyong S (2020) New antimicrobial phenyl alkenoic acids isolated from an oil palm rhizosphere-associated actinomycete, Streptomyces palmae CMU-AB204T. Microorganisms. https://doi.org/10.3390/microorganisms8030350

    Article  PubMed  PubMed Central  Google Scholar 

  7. Djemouai N, Meklat A, Yekkour A, Verheecke-Vaessen C (2023) Actinobacteria: an underestimated source of potential microbial biocontrol agents against fusarium-related diseases in cultivated crops. Eur J Plant Pathol. https://doi.org/10.1007/s10658-023-02737-5

    Article  Google Scholar 

  8. El-Shatoury SA, Ameen F, Moussa H, Abdul Wahid O, Dewedar A, AlNadhari S (2020) Biocontrol of chocolate spot disease (Botrytis cinerea) in faba bean using endophytic actinomycetes Streptomyces: a field study to compare application techniques. PeerJ 8:e8582. https://doi.org/10.7717/peerj.8582

    Article  PubMed  PubMed Central  Google Scholar 

  9. Evangelista-Martínez Z, Contreras-Leal EA, Corona-Pedraza LF, Gastélum-Martínez É (2020) Biocontrol potential of Streptomyces sp. CACIS-1.5CA against phytopathogenic fungi causing postharvest fruit diseases. Egypt J Biol Pest Control. https://doi.org/10.1186/s41938-020-00319-9

    Article  Google Scholar 

  10. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Meier-Kolthoff JP et al (2016) Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 80:1–43. https://doi.org/10.1128/MMBR.00019-15

    Article  PubMed  Google Scholar 

  11. Hu X, Cheng B, Du D, Huang Z, Pu Z, Chen G et al (2019) Isolation and identification of a marine actinomycete strain and its control efficacy against citrus green and blue moulds. Biotechnol Biotechnol Equip 33:719–729. https://doi.org/10.1080/13102818.2019.1613175

    Article  CAS  Google Scholar 

  12. Trinidad-Cruz JR, Rincón-Enríquez G, Evangelista-Martínez Z, Guízar-González C, Enríquez-Vara JN, López-Pérez L et al (2021) Actinobacteria from avocado rhizosphere: antagonistic activity against Colletotrichum gloeosporioides and Xanthomonas sp. Terra Latinoamericana. https://doi.org/10.28940/TERRA.V39I0.802

  13. Palafox-Félix M, Huerta-Ocampo JÁ, Hernández-Ortíz M, Encarnación-Guevara S, Vázquez-Moreno L, Guzmán-Partida AM et al (2022) Proteomic analysis reveals the metabolic versatility of Amycolatopsis sp. BX17: a strain native from milpa agroecosystem soil. J Proteomics 253:104461. https://doi.org/10.1016/j.jprot.2021.104461

    Article  CAS  PubMed  Google Scholar 

  14. Tian H, Shafi J, Ji M, Bi Y, Yu Z (2017) Antimicrobial metabolites from Streptomyces sp. SN0280. J Nat Prod 80:1015–1019. https://doi.org/10.1021/acs.jnatprod.6b01016

    Article  CAS  PubMed  Google Scholar 

  15. Qi D, Zou L, Zhou D, Chen Y, Gao Z, Feng R et al (2019) Taxonomy and broad-spectrum antifungal activity of Streptomyces sp. SCA3–4 isolated from rhizosphere soil of Opuntia stricta. Front Microbiol 10:1390. https://doi.org/10.3389/fmicb.2019.01390

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zheng X, Wang J, Chen Z, Zhang H, Wang Z, Zhu Y et al (2019) A Streptomyces sp. strain: Isolation, identification, and potential as a biocontrol agent against soilborne diseases of tomato plants. Biol Control. https://doi.org/10.1016/j.biocontrol.2019.104004

    Article  Google Scholar 

  17. Jing T, Zhou D, Zhang M, Yun T, Qi D, Wei Y et al (2020) Newly isolated Streptomyces sp. JBS5–6 as a potential biocontrol agent to control banana fusarium wilt: genome sequencing and secondary metabolite cluster profiles. Front Microbiol 11:602591. https://doi.org/10.3389/fmicb.2020.602591

    Article  PubMed  PubMed Central  Google Scholar 

  18. Sharma M, Manhas RK (2020) Purification and characterization of salvianolic acid B from Streptomyces sp. M4 possessing antifungal activity against fungal phytopathogens. Microbiol Res 237:126478. https://doi.org/10.1016/j.micres.2020.126478

    Article  CAS  PubMed  Google Scholar 

  19. Wei Y, Zhao Y, Zhou D, Qi D, Li K, Tang W et al (2020) A newly isolated Streptomyces sp. YYS-7 with a broad-spectrum antifungal activity improves the banana plant resistance to Fusarium oxysporum f. sp. cubense Tropical Race 4. Front Microbiol. https://doi.org/10.3389/fmicb.2020.01712

    Article  PubMed  PubMed Central  Google Scholar 

  20. Gómez ÁG, Ramos FA, Sinuco DC (2021) Screening of volatile organic compounds from Actinobacteria for the control of phytopathogen Colletotrichum gloeosporioides. Biocontrol Sci Technol 31:1067–1079. https://doi.org/10.1080/09583157.2021.1918635

    Article  Google Scholar 

  21. Li X, Jing T, Zhou D, Zhang M, Qi D, Zang X et al (2021) Biocontrol efficacy and possible mechanism of Streptomyces sp. H4 against postharvest anthracnose caused by Colletotrichum fragariae on strawberry fruit. Postharvest Biol Technol. https://doi.org/10.1016/j.postharvbio.2020.111401

    Article  Google Scholar 

  22. Alipour Kafi S, Karimi E, Akhlaghi Motlagh M, Amini Z, Mohammadi A, Sadeghi A (2021) Isolation and identification of Amycolatopsis sp. strain 1119 with potential to improve cucumber fruit yield and induce plant defense responses in commercial greenhouse. Plant Soil 468:125–145. https://doi.org/10.1007/s11104-021-05097-3

    Article  CAS  Google Scholar 

  23. Pérez-Corral DA, de Jesús O-P, Olivas-Orozco GI, Acosta-Muñiz CH, Salas-Marina MÁ, Berlanga-Reyes DI et al (2022) Molecular, morphological and biochemical characterization of actinomycetes and their antagonistic activity against phytopathogenic fungi. Rev Fitotec Mex 45:103–115. https://doi.org/10.35196/rfm.2022.1.103

    Article  Google Scholar 

  24. Allali K, Goudjal Y, Zamoum M, Bouznada K, Sabaou N, Zitouni A (2019) Nocardiopsis dassonvillei strain MB22 from the Algerian Sahara promotes wheat seedlings growth and potentially controls the common root rot pathogen Bipolaris sorokiniana. J Plant Pathol 101:1115–1125. https://doi.org/10.1007/s42161-019-00347-x

    Article  Google Scholar 

  25. Djebaili R, Pellegrini M, Ercole C, Farda B, Kitouni M, Del Gallo M (2021) Biocontrol of soil-borne pathogens of Solanum lycopersicum L. and Daucus carota L. by plant growth-promoting actinomycetes: in vitro and in planta antagonistic activity. Pathogens. https://doi.org/10.3390/pathogens10101305

    Article  PubMed  PubMed Central  Google Scholar 

  26. Guesmi S, Mahjoubi M, Pujic P, Cherif A, Normand P, Sghaier H et al (2022) Biotechnological potential of Kocuria rhizophila PT10 isolated from roots of Panicum turgidum. Int J Environ Sci Technol. https://doi.org/10.1007/s13762-021-03824-y

    Article  Google Scholar 

  27. Li Y, He F, Lai H, Xue Q (2017) Mechanism of in vitro antagonism of phytopathogenic Scelrotium rolfsii by actinomycetes. Eur J Plant Pathol 149:299–311. https://doi.org/10.1007/s10658-017-1177-x

    Article  CAS  Google Scholar 

  28. Thampi A, Bhai RS (2017) Rhizosphere Actinobacteria for combating Phytophthora capsici and Sclerotium rolfsii, the major soil borne pathogens of black pepper (Piper nigrum L.). Biol Control 109:1–13. https://doi.org/10.1016/j.biocontrol.2017.03.006

    Article  CAS  Google Scholar 

  29. Nguyen P-A, Strub C, Durand N, Alter P, Fontana A, Schorr-Galindo S (2018) Biocontrol of Fusarium verticilioides using organic amendments and their actinomycete isolates. Biol Control 118:55–66. https://doi.org/10.1016/j.biocontrol.2017.12.006

    Article  CAS  Google Scholar 

  30. Yang Y, Zhang S-W, Li K-T (2019) Antagonistic activity and mechanism of an isolated Streptomyces corchorusii stain AUH-1 against phytopathogenic fungi. World J Microbiol Biotechnol 35:145. https://doi.org/10.1007/s11274-019-2720-z

    Article  CAS  PubMed  Google Scholar 

  31. Liu C, Zhuang X, Yu Z, Wang Z, Wang Y, Guo X et al (2019) Community structures an antifungal activity of root-associeted andophytic Actinobacteria of healthy and diseased soybean. Microorganisms. https://doi.org/10.3390/microorganisms7080243

    Article  PubMed  PubMed Central  Google Scholar 

  32. Kaur T, Rani R, Manhas RK (2019) Biocontrol and plant growth promoting potential of phylogenetically new Streptomyces sp. MR14 of rhizospheric origin. AMB Express 9:125. https://doi.org/10.1186/s13568-019-0849-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Shariffah-Muzaimah SA, Idris AS, Nur-Rashyeda R, Naidu Y, ZainolHilmi NH, Norman K (2020) Impact of pre-inoculating soil with Streptomyces sp. GanoSA1 on oil palm growth and ganoderma disease development. Biocatal Agric Biotechnol. https://doi.org/10.1016/j.bcab.2020.101814

    Article  Google Scholar 

  34. Gao Y, Zeng XD, Ren B, Zeng JR, Xu T, Yang YZ et al (2020) Antagonistic activity against rice blast disease and elicitation of host-defence response capability of an endophytic Streptomyces albidoflavus OsiLf-2. Plant Pathol 69:259–271. https://doi.org/10.1111/ppa.13118

    Article  CAS  Google Scholar 

  35. Zambrano EC, Parra AS, Ortiz ÁMM (2021) Biocontrol of rice sheath blight with microorganisms obtained in rice cultivated soils. Bragantia. https://doi.org/10.1590/1678-4499.20200356

    Article  Google Scholar 

  36. El-Shanshoury AE-RR, Metwally MA, El-Sabbagh SM, Saba HAE (2022) Biocontrol of Aspergillus flavus Producing Aflatoxin B1 by Streptomyces exfoliatus. Egypt J Bot. https://doi.org/10.21608/ejbo.2022.7763.1287

    Article  Google Scholar 

  37. Kisil OV, Efimenko TA, Efremenkova OV (2021) Looking back to Amycolatopsis: history of the antibiotic discovery and future prospects. Antibiotics (Basel). https://doi.org/10.3390/antibiotics10101254

    Article  PubMed  PubMed Central  Google Scholar 

  38. Yoon J-H, Park Y-H (2006) The Genus Nocardioides. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The Prokaryotes: Volume 3: Archaea Bacteria: Firmicutes, Actinomycetes. Springer New York, New York, NY, pp 1099–1113. https://doi.org/10.1007/0-387-30743-5_44

    Chapter  Google Scholar 

  39. Bennur T, Ravi Kumar A, Zinjarde SS, Javdekar V (2016) Nocardiopsis species: a potential source of bioactive compounds. J Appl Microbiol 120:1–16. https://doi.org/10.1111/jam.12950

    Article  CAS  PubMed  Google Scholar 

  40. Sayed AM, Abdel-Wahab NM, Hassan HM, Abdelmohsen UR (2020) Saccharopolyspora: an underexplored source for bioactive natural products. J Appl Microbiol 128:314–329. https://doi.org/10.1111/jam.14360

    Article  CAS  PubMed  Google Scholar 

  41. Dotis J, Printza N, Stabouli S, Papachristou F (2015) Kocuria species peritonitis: although rare, we have to care. Perit Dial Int 35:26–30. https://doi.org/10.3747/pdi.2013.00138

    Article  PubMed  PubMed Central  Google Scholar 

  42. Quinn GA, Banat AM, Abdelhameed AM, Banat IM (2020) Streptomyces from traditional medicine: sources of new innovations in antibiotic discovery. J Med Microbiol 69:1040–1048. https://doi.org/10.1099/jmm.0.001232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Song Z, Xu T, Wang J, Hou Y, Liu C, Liu S et al (2021) Secondary metabolites of the genus Amycolatopsis: structures, bioactivities, biosynthesis. Molecules. https://doi.org/10.3390/molecules26071884

    Article  Google Scholar 

  44. Evseev P, Lukianova A, Tarakanov R, Tokmakova A, Shneider M, Ignatov A et al (2022) Curtobacterium spp. and Curtobacterium flaccumfaciens: phylogeny, genomics-based taxonomy, pathogenicity, and diagnostics. Curr Issues Mol Biol 44:889–927. https://doi.org/10.3390/cimb44020060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Lee N, Hwang S, Lee Y, Cho S, Palsson B, Cho B-K (2019) Synthetic biology tools for novel secondary metabolite discovery in Streptomyces. J Microbiol Biotechnol 29:667–686. https://doi.org/10.4014/jmb.1904.04015

    Article  CAS  PubMed  Google Scholar 

  46. Gomes ES, Schuch V, de Macedo Lemos EG (2013) Biotechnology of polyketides: new breath of life for the novel antibiotic genetic pathways discovery through metagenomics. Braz J Microbiol 44:1007–1034. https://doi.org/10.1590/s1517-83822013000400002

    Article  CAS  PubMed  Google Scholar 

  47. Mitra D, Mondal R, Khoshru B, Senapati A, Radha TK, Mahakur B et al (2022) Actinobacteria-enhanced plant growth, nutrient acquisition, and crop protection: Advances in soil, plant, and microbial multifactorial interactions. Pedosphere 32:149–170. https://doi.org/10.1016/S1002-0160(21)60042-5

    Article  CAS  Google Scholar 

  48. Sarwar A, Hassan MN, Imran M, Iqbal M, Majeed S, Brader G et al (2018) Biocontrol activity of surfactin A purified from Bacillus NH-100 and NH-217 against rice bakanae disease. Microbiol Res 209:1–13. https://doi.org/10.1016/j.micres.2018.01.006

    Article  CAS  PubMed  Google Scholar 

  49. Wan C, Fan X, Lou Z, Wang H, Olatunde A, Rengasamy KRR (2022) Iturin: cyclic lipopeptide with multifunction biological potential. Crit Rev Food Sci Nutr 62:7976–7988. https://doi.org/10.1080/10408398.2021.1922355

    Article  CAS  PubMed  Google Scholar 

  50. Martínez-Núñez MA, López VEL y (2016) Nonribosomal peptides synthetases and their applications in industry. Sustain Chem Process 4:1–8. https://doi.org/10.1186/s40508-016-0057-6

    Article  CAS  Google Scholar 

  51. Maier F, Zwicker S, Hückelhoven A, Meissner M, Funk J, Pfitzner AJP et al (2011) Nonexpressor of pathogenesis-related proteins1 (NPR1) and some NPR1-related proteins are sensitive to salicylic acid. Mol Plant Pathol 12:73–91. https://doi.org/10.1111/j.1364-3703.2010.00653.x

    Article  CAS  PubMed  Google Scholar 

  52. Liotti RG, da Silva Figueiredo MI, Soares MA (2019) Streptomyces griseocarneus R132 controls phytopathogens and promotes growth of pepper (Capsicum annuum). Biol Control. https://doi.org/10.1016/j.biocontrol.2019.104065

    Article  Google Scholar 

  53. Boro M, Sannyasi S, Chettri D, Verma AK (2022) Microorganisms in biological control strategies to manage microbial plant pathogens: a review. Arch Microbiol 204:666. https://doi.org/10.1007/s00203-022-03279-w

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

To Universidade Federal do Rio Grande do Sul for the opportunity to development of this work and to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support.

Funding

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Case Number: 88887.463460/2019-00.

Author information

Authors and Affiliations

  1. Departamento de Microbiologia, Imunologia e Parasitologia, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul (UFRGS), Ramiro Barcelos 2600, Porto Alegre, RS, 90035-003, Brazil

    Heloísa Giacomelli Ribeiro & Sueli Teresinha Van Der Sand

Authors
  1. Heloísa Giacomelli Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sueli Teresinha Van Der Sand
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. The first draft of the manuscript was written by Heloísa Giacomelli Ribeiro and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sueli Teresinha Van Der Sand.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest regarding the publication of this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giacomelli Ribeiro, H., Teresinha Van Der Sand, S. Exploring the Trends in Actinobacteria as Biological Control Agents of Phytopathogenic Fungi: A (Mini)-Review. Indian J Microbiol 64, 70–81 (2024). https://doi.org/10.1007/s12088-023-01166-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12088-023-01166-6

Keywords

Search

Navigation