journal article·2022-11-10Open access

Streptomyces spp. Biofilmed Solid Inoculant Improves Microbial Survival and Plant-Growth Efficiency of Triticum aestivum

Karla Gabriela Domínguez-González, J. Jesús Robledo-Medrano, Juan José Valdez-Alarcón, Orlando Hernández-Cristobal, Héctor Eduardo Martínez-Flores, Jorge Francisco Cerna-Cortés, Ma. Guadalupe Garnica-Romo, Raúl Cortés-Martínez

Applied Sciences· Volume 12· Issue 22

Abstract

Streptomyces species have been successfully used in diverse biotechnological processes; however, little is known about actinobacterial biofilm formation and its use as a biofilmed inoculant. The present study assessed and compared the ability of some plant growth-promoting actinobacterial strains to form biofilms on a carrier to improve microbial survival and colonize the rhizosphere and roots of Triticum aestivum, resulting in positive interactions and benefits to the plant. Forty-one actinobacterial isolates from Persea americana organic rhizosphere farms were tested on plant growth and biofilm-forming capacities, showing their potential use as bio-fertilizers in agriculture. Three Streptomyces strains were selected and tested for biofilm formation and plant growth-promoting (PGP) features. Biofilms were induced on the perlite carrier and used to inoculate seven treatments with T. aestivum in pot essays, resulting in a >200% increase in root weight and a >400% increase in total biomass. Endophytic colonization was achieved in all the treatments. Microbial survival ranged between 108 and 109 CFU/g after 12 weeks of treatment, indicating actinobacterial permanence on the carrier. Successful consortia formation was observed for mixed-strain treatments, suggesting long-term plant recolonization.
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Research context

OpenAlex topics: Plant-Microbe Interactions and Immunity · Legume Nitrogen Fixing Symbiosis · Mycorrhizal Fungi and Plant Interactions

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Facultad de Químico Farmacobiología, Universidad Michoacana de San Nicolás de Hidalgo, Tzintzuntzan 173, Col. Matamoros, Morelia 58240, Michoacán, Mexico

Laboratorio de Epidemiología Molecular y Biotecnología de Enfermedades Infecciosas, Centro Multidisciplinario de Estudios en Biotecnología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Michoacana de San Nicolás de Hidalgo, Km 9.5 Carretera Morelia-Zinapécuaro s/n, Posta Veterinaria. La Palma, Tarímbaro, C.P., Morelia 58893, Michoacán, Mexico

Escuela Nacional de Estudios Superiores (ENES), Unidad Morelia, UNAM. Antigua Carretera a Pátzcuaro 8701, col. Ex Hacienda San José de la Huerta, Morelia 58190, Michoacán, Mexico

Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Prolongación de Carpio, Calle Plan de Ayala s/n, Santo Tomás, Miguel Hidalgo, Ciudad de México 11350, Mexico

Facultad de Ingeniería Civil, Universidad Michoacana de San Nicolás de Hidalgo, Gral. Francisco J. Mújica 172B, Felicitas del Río, Morelia 58040, Michoacán, Mexico

Funding

Coordinación de la Investigación Científica-UMSNH · PRODEP

References (83)

Show source-provided references
1. FAO (2021). The State of Food Security and Nutrition in the World 2021: Transforming Food Systems for Food Security, Improved Nutrition and Affordable Healthy Diets for All, FAO. The State of Food Security and Nutrition in the World (SOFI).
2. Agriculture, Pesticides, Food Security and Food Safety10.1016/j.envsci.2006.08.002 ↗
3. Field Evaluation of Effective Microorganisms (EM) Application for Growth, Nodulation, and Nutrition of Mung Bean
4. Induction of Resistance in Chili against Sclerotium Rolfsii by Plant-Growth-Promoting Rhizobacteria and Anagallis Arvensis10.1186/s41938-021-00364-y ↗
5. Evaluation of Actinomycete Strains for Key Traits Related with Plant Growth Promotion and Mycorrhiza Helping Activities10.1016/j.apsoil.2010.04.007 ↗
6. Ahmad, I., and Husain, F.M. (2017). Role of PGPR in Biofilm Formations and Its Importance in Plant Health. Biofilms in Plant and Soil Health, John Wiley & Sons, Ltd.10.1002/9781119246329 ↗
7. Yadav, M.K., and Singh, B.P. (2020). Chapter 16—Agriculturally Important Microbial Biofilms: Biodiversity, Ecological Significances, and Biotechnological Applications. New and Future Developments in Microbial Biotechnology and Bioengineering: Microbial Biofilms, Elsevier.
8. Yadav, A.N., Singh, J., Rastegari, A.A., and Yadav, N. (2020). Plant Microbiomes for Sustainable Agriculture, Springer Nature.10.1007/978-3-030-38453-1 ↗
9. Ansari, R.A., and Mahmood, I. (2019). Biofilmed Biofertilizer for Sustainable Agriculture. Plant Health Under Biotic Stress: Volume 2: Microbial Interactions, Springer.10.1007/978-981-13-6040-4 ↗
10. Verma, V.C., and Gange, A.C. (2014). Endophytic Actinobacteria: Diversity and Ecology. Advances in Endophytic Research, Springer India.10.1007/978-81-322-1575-2 ↗
11. Subramaniam, G., Arumugam, S., and Rajendran, V. (2016). Actinomycetes Bio-Inoculants: A Modern Prospectus for Plant Disease Management. Plant Growth Promoting Actinobacteria: A New Avenue for Enhancing the Productivity and Soil Fertility of Grain Legumes, Springer.
12. Biofilm Formation in the Life Cycle of the Cellulolytic Actinomycete Thermobifida fusca10.1017/S1479050508002238 ↗
13. Actinomycetes Benefaction Role in Soil and Plant Health10.1016/j.micpath.2017.09.036 ↗
14. Singh, B.P., Gupta, V.K., and Passari, A.K. (2018). Chapter 8—Streptomyces in Plant Growth Promotion: Mechanisms and Role. New and Future Developments in Microbial Biotechnology and Bioengineering, Elsevier.
15. Evaluating the Efficacy of Cyanobacterial Formulations and Biofilmed Inoculants for Leguminous Crops10.1080/03650340.2013.792407 ↗
16. Actinomycetes: Source, Identification, and Their Applications
17. Comparison of the Main Siderophores Produced by Some Species of Streptomyces10.1007/BF00294289 ↗
18. Actinobacteria Associated with Arbuscular Mycorrhizal Funneliformis Mosseae Spores, Taxonomic Characterization and Their Beneficial Traits to Plants: Evidence Obtained from Mung Bean (Vigna radiata) and Thai Jasmine Rice (Oryza sativa)10.3389/fmicb.2018.01247 ↗
19. Effects of Actinobacteria on Plant Disease Suppression and Growth Promotion10.1007/s00253-013-5206-1 ↗
21. Biofilmed Biofertilisers: Novel Inoculants for Efficient Nutrient Use in Plants
22. Biofilmed Biofertilizer: Promising Technology for Tomorrow
23. The Biofilm Matrix10.1038/nrmicro2415 ↗
24. Emergence of Diverse Microbes on Application of Biofilmed Biofertilizers to a Maize Growing Soil10.4038/cjsbs.v42i2.6612 ↗
25. Current Understanding on Adhesion and Biofilm Development in Actinobacteria
26. A Rhizobial Biofilm with Nitrogenase Activity Alters Nutrient Availability in a Soil10.1016/j.soilbio.2005.02.027 ↗
27. Micronutrient Enrichment Mediated by Plant-Microbe Interactions and Rice Cultivation Practices10.1080/01904167.2016.1148723 ↗
28. Effect of Biofilmed Biofertilizer on Plant Growth and Nutrient Uptake of Hevea Brasiliensis Nursery Plants at Field Condition10.4038/jrrisl.v98i0.1873 ↗
29. Importance of Biofilm Formation in Plant Growth Promoting Rhizobacterial Action10.1007/978-3-642-13612-2_4 ↗
30. Fungal-Bacterial Biofilms: Their Development for Novel Biotechnological Applications10.1007/s11274-007-9539-8 ↗
31. Mycelial Colonization by Bradyrhizobia and Azorhizobia10.1007/BF02706224 ↗
32. Tea Yield Maintained in PGPR Inoculated Field Plants despite Significant Reduction in Fertilizer Application10.1016/j.rhisph.2019.100146 ↗
33. Bioformulation of Biochar as a Potential Inoculant Carrier for Sustainable Agriculture10.1016/j.eti.2020.101168 ↗
34. Malusá, E., Sas-Paszt, L., and Ciesielska, J. (2020, October 28). Technologies for Beneficial Microorganisms Inocula Used as Biofertilizers. Available online: https://www.hindawi.com/journals/tswj/2012/491206/.10.1100/2012/491206 ↗
35. Alternatives to Peat as a Carrier for Rhizobia Inoculants: Solid and Liquid Formulations10.1016/j.soilbio.2008.07.021 ↗
36. Effects of Carrier, Sterilisation Method, and Incubation on Survival of Bradyrhizobium japonicum in Soybean (Glycine max L.) Inoculants10.1016/j.enzmictec.2007.06.011 ↗
37. Nutrient Supplementation of Pinewood Biochar for Use as a Bacterial Inoculum Carrier10.1007/s00374-016-1093-9 ↗
38. Kelly, K.L., Judd, D.B., Inter-Society Color Council, and United States National Bureau of Standards (1965). ISCC-NBS Color-Name Charts Illustrated with Centroid Colors.
39. Studies on Isolation, Taxonomy and Ecology of Soil Actinomycetes (in Japanese with English Abstract)10.3209/saj.3_45 ↗
40. Numerical Classification and Identification of Streptomyces Species—A Review10.1016/0378-1119(92)90563-5 ↗
41. 16S Ribosomal DNA Amplification for Phylogenetic Study10.1128/jb.173.2.697-703.1991 ↗
42. Archaea in Coastal Marine Environments10.1073/pnas.89.12.5685 ↗
43. An Efficient Microbiological Growth Medium for Screening Phosphate Solubilizing Microorganisms10.1111/j.1574-6968.1999.tb13383.x ↗
44. Comparison of Colorimetric and ICP Methods of Phosphorus Determination in Soil Extracts10.1080/00103624.2013.832771 ↗
45. A Rapid Method to Determine Total Phosphorus in Soils10.2136/sssaj1988.03615995005200050016x ↗
46. The colorimetric determination of phosphorus10.1016/S0021-9258(18)84756-1 ↗
47. Sommers 1982 Phosphorus10.2134/agronmonogr9.2.2ed.c24 ↗
48. Phosphate Solubilizing Actinomycetes in the Estuarine Environment: An Inventory
49. A Critical Examination of the Specificity of the Salkowski Reagent for Indolic Compounds Produced by Phytopathogenic Bacteria10.1128/aem.61.2.793-796.1995 ↗
50. Role of Pseudomonas Putida Indoleacetic Acid in Development of the Host Plant Root System10.1128/AEM.68.8.3795-3801.2002 ↗
51. Balagurunathan, R., Radhakrishnan, M., Shanmugasundaram, T., Gopikrishnan, V., and Jerrine, J. (2020). Characterization and Identification of Actinobacteria. Protocols in Actinobacterial Research, Springer US. Springer Protocols Handbooks.10.1007/978-1-0716-0728-2 ↗
52. Non-Frankia Actinomycetes Isolated from Surface-Sterilized Roots of Casuarina Equisetifolia Fix Nitrogen10.1128/AEM.71.1.460-466.2005 ↗
53. Thymidine-Requiring Mutants of Phage T410.1073/pnas.50.3.526 ↗
54. Characterization of Siderophore Production by the Biological Control Agent Enterobacter cloacae10.1094/MPMI-7-0440 ↗
55. A Comparative Study of Siderophore Production by Fungi from Marine and Terrestrial Habitats10.1016/j.jembe.2003.12.028 ↗
56. Romeo, T. (2008). Innate and Induced Resistance Mechanisms of Bacterial Biofilms. Bacterial Biofilms, Springer.10.1007/978-3-540-75418-3 ↗
57. Lateral Flagella Are Required for Increased Cell Adherence, Invasion and Biofilm Formation by Aeromonas spp10.1016/S0378-1097(03)00418-X ↗
58. Composición lipídica de la pared celular de tres especies de micobacterias ambientales y su posible correlación con la formación de biofilms y movilidad por sliding/Lipid composition of cell wall of three species of environmental mycobacteria and its po
59. Biofilm Formation as Microbial Development10.1146/annurev.micro.54.1.49 ↗
60. New Method for Detecting Slime Production by Coagulase Negative Staphylococci10.1136/jcp.42.8.872 ↗
61. Modification of the Congo Red Agar Method to Detect Biofilm Production by Staphylococcus epidermidis10.1016/j.diagmicrobio.2012.11.014 ↗
62. Sliding Motility in Mycobacteria10.1128/JB.181.23.7331-7338.1999 ↗
63. Nontuberculous Mycobacteria Pathogenesis and Biofilm Assembly10.1016/j.ijmyco.2014.11.065 ↗
64. Improved Culturability of Soil Bacteria and Isolation in Pure Culture of Novel Members of the Divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia10.1128/AEM.68.5.2391-2396.2002 ↗
65. Isolation and Identification of Actinobacteria from Surface-Sterilized Wheat Roots10.1128/AEM.69.9.5603-5608.2003 ↗
66. Effect of Plant Growth-Promoting Streptomyces sp. on Plant Growth and Yield of Tomato and Chilli
67. Enhancing Pomegranate (Punica granatum L.) Plant Health through the Intervention of a Streptomyces Consortium10.1080/09583157.2020.1859095 ↗
68. Boubekri, K., Soumare, A., Mardad, I., Lyamlouli, K., Hafidi, M., Ouhdouch, Y., and Kouisni, L. (2021). The Screening of Potassium- and Phosphate-Solubilizing Actinobacteria and the Assessment of Their Ability to Promote Wheat Growth Parameters. Microorganisms, 9.10.3390/microorganisms9030470 ↗
69. Bioinformatic and Functional Evaluation of Actinobacterial Piperazate Metabolism10.1021/acschembio.8b01086 ↗
70. Biological Control and Plant Growth-Promotion Traits of Streptomyces Species Under Greenhouse and Field Conditions in Chickpea10.1007/s40003-017-0278-2 ↗
71. A Review on Streptomyces spp. as Plant-Growth Promoting Bacteria (PGPB)
72. Actinomycetes Producing Anti-Methicillin Resistant Staphylococcus aureus from Soil Samples in Nakhon Si Thammarat
73. Emerging Trends in the Discovery of Natural Product Antibacterials10.1016/j.coph.2013.07.002 ↗
74. Wang, W., Feng, M., Li, X., Chen, F., Zhang, Z., Yang, W., Shao, C., Tao, L., and Zhang, Y. (2022). Antibacterial Activity of Aureonuclemycin Produced by Streptomyces aureus Strain SPRI-371. Molecules, 27.10.3390/molecules27155041 ↗
75. Biodegradation of Deltamethrin and Its Hydrolysis Product 3-Phenoxybenzaldehyde by a Newly Isolated Streptomyces aureus Strain HP-S-0110.1007/s00253-011-3136-3 ↗
76. Enhancement of Cypermethrin Degradation by a Coculture of Bacillus cereus ZH-3 and Streptomyces aureus HP-S-0110.1016/j.biortech.2012.01.106 ↗
77. Mechanism of Phosphate Solubilization and Antifungal Activity of Streptomyces spp. Isolated from Wheat Roots and Rhizosphere and Their Application in Improving Plant Growth10.1099/mic.0.074146-0 ↗
78. Perlite as a Carrier for Bacterial Inoculants10.1016/S0038-0717(99)00185-6 ↗
79. Long-Term Storage of Collection Cultures of Actinobacteria10.1134/S0026261712050062 ↗
80. A Quantitative Review of the Effects of Biochar Application to Soils on Crop Productivity Using Meta-Analysis10.1016/j.agee.2011.08.015 ↗
81. Biochar and Its Effects on Plant Productivity and Nutrient Cycling: A Meta-Analysis10.1111/gcbb.12037 ↗
82. Biochar Induced Soil Microbial Community Change: Implications for Biogeochemical Cycling of Carbon, Nitrogen and Phosphorus10.1016/j.pedobi.2011.07.005 ↗
83. Streptomyces sp. ASBV-1 Reduces Aflatoxin Accumulation by Aspergillus parasiticus in Peanut Grains10.1111/j.1365-2672.2008.03940.x ↗