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Biotechnological potential of bacteria from genera Bacillus Paraburkholderia and Pseudomonas to control seed fungal pathogens

  • Environmental Microbiology - Research Paper
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Abstract

Fungal pathogens are important determinants of plant dynamics in the environment. These pathogens can cause plant death and occasionally yield losses in crops, even at low initial densities in the soil. The objective of this study was to select and evaluate fungal antagonistic bacteria and to determine their biological control capacity in soybean seedlings. A total of 877 strains from the genera Pseudomonas, Bacillus, and Paraburkholderia/Burkholderia were screened, and their antagonistic effects on fungi frequently found in seeds were evaluated using four methods: quadruple plating, paired culture confrontation, strain containment, and inoculation of soybean seeds. The experimental design was completely randomized, with three replications for the first three methods and five replications in a 3 × 9 factorial scheme for the fourth treatment. The strains with the highest biotechnological potential were inoculated into soybean seeds to evaluate the biological control of fungi that attack this crop at germination. Seventy-nine strains presented some type of antagonistic effect on the tested fungi, with two strains presenting a broader antagonistic action spectrum in the seed test. In addition to the antagonistic potential, strains BR 10788 and BR 11793, when simultaneously inoculated or alone, significantly increased the seedling dry matter mass, and promoted the growth of soybean seedlings even in the presence of most fungi. Thus, this study demonstrated the efficiency of the antagonistic activity of these strains in relation to the target fungi, which proved to be potential agents for biological control.

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References

  1. Deacon JW (1991) Significance of ecology in the development of biocontrol agents against soil-borne plant pathogens. Biocontrol Sci Technol 1:5–20

    Google Scholar 

  2. Pliego C, Ramos C, de Vicente A, Cazorla F (2011) Screening for candidate bacterial biocontrol agents against soilborne fungal plant pathogens. Plant Soil 340:505–520

    CAS  Google Scholar 

  3. Braga Junior GM, Chagas Junior AF, Chagas LFB, de Carvalho Filho MR, Miller LO, dos Santos GR (2017) Controle biológico de fitopatógenos por Bacillus subtilis in vitro. Biota Amazônia Open Journal System – Macapá 7(3):45–51

    Google Scholar 

  4. Bettiol W (1999) Controle biológico de doenças. Ação Ambiental 2:30–33

    Google Scholar 

  5. Santos MSB, Silva AACR (2014) Sanidade de sementes de arroz, biocontrole, caracterização e transmissão de Curvularia lunata em semente-plântula de arroz. Revista Ceres 61(4):511–517

    Google Scholar 

  6. Vinale F, Abadi K, Ruocco M, Marra R, Scala F, Zoina A, Woo S, Lorito M (2003) Remediation of pollution by using biological systems based on beneficial plant-microorganisms interactions. Journal of Plant Pathology 85(4):301 https://scholar.google.com.br/scholar?start=70&q=Vinale&hl=pt-BR&as_sdt=0,5#d=gs_qabs&u=%23p%3DGygbAOdjotYJ

    Google Scholar 

  7. Melo IS (1998) Agentes Microbianos de Controle de Fungos Fitopatogênicos. In: Melo IS, Azevedo JL (eds) Controle Biológico. 1. Embrapa Meio Ambiente, Jaguariúna, pp 17–67

    Google Scholar 

  8. Blum BJ (2007) Concepts and Strategies for a successful product development: the industry’s development concept. In: Cost Action 850 – Conference Schloss Salzau, Germany

  9. Guedes, AC, Goedert CO, Bustamante PG, Moreira JRA, Mariante AS, Walter BMT, Brandão CRF, Proença CEB, Munhoz CBR, Magalhães C, Silva GP, Colli GR, Branchetti L, Mendes MS, Veiga R, Mendonça RC, Silva SR, Cavalcanti, TB, Pereira TS (2004) Estratégia Nacional de Diversidade Biológica. Conservação ex situ

  10. Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Ann Rev Phytopathol 40:309–348

    CAS  Google Scholar 

  11. Morandi MAB, Paula Júnior TJ, Bettiol W, Teixeira H (2009) Controle biológico de pragas, doenças e plantas invasoras. Informe Agropecuário, Belo Horizonte 30(251):73–82 jul/ago

    Google Scholar 

  12. Bressan W (2003) Biological control of maize seed pathogenic fungi by use of actinomycetes. Biocontrol 48:233–240

    Google Scholar 

  13. Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359

    CAS  PubMed  Google Scholar 

  14. Peixoto-Neto PAS, Azevedo JL, Araújo WL (2002) Microrganismos endofíticos: interação com plantas e potencial biotecnológico. Biotecnologia, Ciência & Desenvolvimento 29:62–76

    Google Scholar 

  15. Pérez C, Muñoz-Garay C, Portugal LC, Sánchez J, Gill SS, Soberón M, Bravo A (2007) Bacillus thuringiensis ssp. israelensis Cyt1Aa enhances activity of Cry11Aa toxin by facilitating the formation of a pre-pore oligomeric structure. Cell Microbiol 9:2931–2937

    PubMed  PubMed Central  Google Scholar 

  16. Govindasamy V, Senthilkumar M, Magheshwaran V, Kumar U, Bose P, Sharma V, Annapurna K (2011) Bacillus and Paenibacillus spp: Potential PGPR for Sustainable Agriculture. In: Maheshwari DK (ed) Plant Growth and Health Promoting Bacteria. Springer, Berlin Heidelberg, pp 333–364

    Google Scholar 

  17. Velho RV, Caldas DGG, Medina LFC, Tsai SM, Brandelli A (2011) Real-time PCR investigation on the expression. Of sboA and ituD genes in Bacillus spp. Letters in Applied Microbiology 52:660–666

    CAS  PubMed  Google Scholar 

  18. Rückert C, Blom J, Chen X, Reva O, Borriss R (2011) Genome sequence of B. amyloliquefaciens type strain DSM7T reveals differences to plant-associated B. amyloliquefaciens FZB42. J Biotechnol 155:78–85

    PubMed  Google Scholar 

  19. Kumar KVK, Yellareddygari SKR, Reddy MS, Kloepper JW, Lawrence KS, Zhou XG, Sudini H, Groth DE, Raju SK, Miller ME (2012) Efficacy of Bacillus subtilis MBI 600 against shealth blight caused by Rhizoctonia solani and on growth and yield of rice. Rice Science 19(1):55–63

    Google Scholar 

  20. Chen J, Wang X, Han H (2013) A new function of graphene oxide emerges: inactivating phytopathogenic bacterium Xanthomonas oryzae pv. Oryzae. Journal of Nanoparticle Research 15(5):1658 https://link.springer.com/article/10.1007/s11051-013-1658-6

    Google Scholar 

  21. Chowdhury SP, Dietel K, Rändler M, Schmid M, Junge H, Borriss R (2013) Effects of Bacillus amyloliquefaciens FZB42 on lettuce growth and health under pathogen pressure and its impact on the rhizosphere bacterial community. PLoS ONE 8:e68818. https://doi.org/10.1371/journal.pone.0068818

    Article  PubMed  PubMed Central  Google Scholar 

  22. Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. https://doi.org/10.1111/j.1574-6976.2010.00221.x

    Article  CAS  PubMed  Google Scholar 

  23. Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genetics and Molecular Biology 35(suppl 4):1044–1051

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Khan N, Maymon M, Hirsch AM (2017) Combating Fusarium Infection Using Bacillus-Based Antimicrobials. Microorganisms 5:75. https://doi.org/10.3390/microorganisms5040075

    Article  CAS  PubMed Central  Google Scholar 

  25. Sawana A, Adeolu M, Gupta RS (2014) Molecular signatures and phylogenomic analysis of the genus Burkholderia: Proposal for division of this genus into the emended genus Burkholderia containing pathogenic organisms and a new genus Paraburkholderia gen. nov. harboring environmental species. Frontiers in Genetics 5:429

    PubMed  PubMed Central  Google Scholar 

  26. Miotto-Vilanova L, Jacquard C, Courteaux B, Wortham L, Michel J, Clément C, Barka EA, Sanchez L (2016) Burkholderia phytofirmans PsJN confers grapevine resistance against Botrytis cinerea via a direct antimicrobial effect combined with a better resource mobilization. Front Plant Sci 7:1236. https://doi.org/10.3389/fpls.2016.01236

    Article  PubMed  PubMed Central  Google Scholar 

  27. Eberl L, Vandamme P (2016) Members of the genus Burkholderia: Good and bad guys. F1000. Research 5:1007

    Google Scholar 

  28. Dias GM, Pires AS, Grilo VS, Castro MR, Vilela LF, Neves BC (2019) Comparative genomics of Paraburkholderia kururiensis and its potential in bioremediation, biofertilization, and biocontrole of plant pathogens. Microbiol Open

  29. Vitorino LC, Bessa LA (2017) Technological microbiology: Development and applications. Frontiers in Microbiology 8:827

    PubMed  PubMed Central  Google Scholar 

  30. Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of Plant Growth by Bacterial ACC Deaminase. Critical Reviews in Plant Sciences 26:227–242

    CAS  Google Scholar 

  31. Yang JO, Kim WY, Bhak J (2009) ssSNPTarget: genome-wide splice-site single nucleotide polymorphism database. Human Mutation 30:E1010E1020

    Google Scholar 

  32. Andreolli M, Lampis S, Zapparoli G, Angelini E, Vallini G (2016) Diversity of bacterial endophytes in 3 and 15 years-old grapevines of Vitis vinífera cv. Corvina and their potential for plant growth promotion and phytophatogen control. Microbiol Res 183:42–52

    PubMed  Google Scholar 

  33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Vergara C, Araújo KEC, Urquiara S, Schultz, N, Balieiro FC, Medeiros PS, Santos LA, Xavier GR, Zilli JE (2017) Dark septate endophytic fungi help tomato to arquire nutrients from ground plant material. Front Microbiol 8

  35. Mariano RLR (1993) Métodos de seleção “in vitro” para controle microbiológico. Revista Anual Patologia de Plantas 1:369–409

    Google Scholar 

  36. Tullio HE (2017) Potencial de bactérias endofíticas do cacau para o controle de fungos de solo e promoção de crescimento radicular na cultura da soja. Dissertação, Universidade Estadual de Ponta Grossa, Paraná, Brazil

  37. Scheidt W, Pedroza ICPS, Fontana J, Meleiro LAC, Soares LHB, Reis VM (2019) Optimization of culture medium and growth conditions of the plant growth-promoting bacterium Herbaspirillum seropedicae BR11417 for its use as an agricultural inoculant using response surface methodology (RSM). Plant Soil 451:75–87

    Google Scholar 

  38. Luz WC (2001) Efeito de bioprotetores em patógenos de sementes e na emergência e rendimento de grãos de milho. Fitopatologia Brasileira 26:1

    Google Scholar 

  39. los Santos P E-d, Palmer M, Chávez-Ramírez B, Beukes C, Steenkamp ET, Bricoe L, Khan N, Mulak M, Lafos M, Humm E, Arrabit M, Crook M, Gross E, Simon MF, dos Reis FB Jr, Whitman WB, Nicole S, Poole PS, Hirsch AM, Venter SN, James EK (2018) Whole Genome Analyses Suggests thar Burkholderia sensu lato Contains Two Additional Novel Genra (Mycetohabitans gen. nov., and Trinickia gen. nov.): Implication for the Evolution of Diazotrophy and Nodulation in the Burkholderiaceae. Genes 9:389

    Google Scholar 

  40. Kobayashi DY, Reedy RM, Bick JA, Oudemans PV (2002) Characterization of a chitinase gene from Stenotrophomonas maltophilia strain 34 S1 and its involvement in biological control. Appl Environ Microbiol 68:1047–1054

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Raaijmakers JM, Vlami M, de Souza JT (2002) Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek 81:537–547

    CAS  PubMed  Google Scholar 

  42. Gross H, Loper JE (2009) Genomic of secondary metabolite production by Pseudomonas spp. Nat Prod Rep 26:1408–1446

    CAS  PubMed  Google Scholar 

  43. Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany 52:487–511

    CAS  PubMed  Google Scholar 

  44. Zucchi TD (2007) Potencial de linhagens de Bacillus subtilis, Paenibacillus lentimorbus e Streptomyces sp. no controle de fungos aflatoxigênicos em amendoim (Arachis hypogaea) e aspectos de biossegurança. Tese, Universidade de São Paulo, São Paulo, Brazil

  45. Lima ODDR, dos Santos MSB, Rodrigues AAC (2014) Ação antifúngica in vitro de isolados de Bacillus ssp. sobre Fusarium oxysporum f. sp. lycopersici. Revista Caatinga 27(4):57–64

    Google Scholar 

  46. Matsuno Y, Ano T, Shoda M (1992) Cloning of a gene responsible for the specific production of an antifungal antibiotic iturin with n-C16-b-amino acid residue. Journal of General and Applied Microbiology 38:505–509

    CAS  Google Scholar 

  47. Bettiol W, Kimati H (1990) Efeito de Bacillus subtilis subtilis sobre Pyricularia oryzae agente causal de bruzone do arroz. Pesquisa Agropecuária Brasileiro 25:1165–1174

    Google Scholar 

  48. Furlan SH, Verchaito MH (2005) Efeito de Bacillus subtilis e Trichoderma sp. no tratamento de sementes de feijão visando o controle de Colletotrichum lindemuthianum. In: Congresso Nacional de Pesquisa de Feijão, 7, Santo Antônio de Goiás. Anais... Santo Antônio de Goiás: Embrapa Arroz e Feijão, Documentos 182, vol 1, pp 182–185

  49. Araújo FF, Henning A, Hungria M, de Lima J (1995) Caracterização do potencial antifúngico de Bacillus spp. isolados de solos do Paraná. In: Hungria M, Balota EL, Colozzi-Filho A, Andrade DS (eds) Microbiologia do solo: desafios para o século XXI. Iapar/Embrapa-CNPSo, Londrina, pp 450–455

    Google Scholar 

  50. Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: Molecular plant-rhizobacteria interactions. Plant Cell and Environment 26:186–199

    Google Scholar 

  51. Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Applied Biochemistry and Microbiology, New York 42(2):117–126

    CAS  Google Scholar 

  52. Kimati H, Gimenez-Fernandes N, Soave J, Kurozawa C, Brignani Neto F, Bettiol W (1997) Guia de Fungicidas Agrícolas – Recomendações por Cultura, v. 1, 2ª ed. Jaboticabal, Grupo Paulista de Fitopatologia, 225p

  53. Kondoh M, Hirai M, Shoda M (2001) Integrated biological and chemical control of damping-off caused by Rhizoctonia solaniu using Bacillus subtilis IXB14-C and Flutolanil. Journal of Bioengineering 91(2):173–177

    CAS  Google Scholar 

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We thank Dr. Goulart, ACP (Embrapa Agropecuária Oeste) for providing the fungi for the study. We also thank the CNPq (Brazilian National Council for Scientific and Technological Development) and Capes (Coordination for the Improvement of Higher Education Personnel) for the grants awarded to some of the authors and financial support of projects, especially INCT Plant Growth–Promoting Microorganisms for Agricultural Sustainability and Environmental Responsibility (465133/2014-2).

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Correspondence to Jerri Édson Zilli.

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Fernandes, M.F.R., Ribeiro, T.G., Rouws, J.R. et al. Biotechnological potential of bacteria from genera Bacillus Paraburkholderia and Pseudomonas to control seed fungal pathogens. Braz J Microbiol 52, 705–714 (2021). https://doi.org/10.1007/s42770-021-00448-9

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