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Streptomyces sp. CLV45 from Fabaceae rhizosphere benefits growth of soybean plants

  • Environmental Microbiology - Research Paper
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Abstract

Plant growth-promoting bacteria such as Streptomyces are an attractive alternative for increasing the sustainability of agricultural systems. In this study, Streptomyces isolates obtained from rhizosphere soil of plants in the family Fabaceae were characterized for their plant growth-promoting traits, including the production of siderophores, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, indole-3-acetic acid (IAA), and phenazines. Soybean seeds were bacterized with selected isolates to test growth promotion. All isolates produced IAA, and the isolate CLV45 was the most efficient, reaching 398.53 mg of IAA per gram of cells. CLV41, CLV45, and CLV46 showed high activity for ACC deaminase whereas CLV42, CLV44, and CLV46 were efficient in siderophore production. Pyocyanin was detected in all isolates; CLV41, CLV43, and CLV45 produced phenazine-carboxylic acid as well. Selected for IAA and ACC deaminase production combined with production of siderophores and phenazines, CLV42, CLV44, and CLV45 were tested for their growth promotion potential. Seed bacterization with CLV45 resulted in plants with increased shoot growth (36.63%) and dry mass (17.97%) compared to control plants. Results suggest that moderate or high levels of auxin and ACC deaminase production by the isolate CLV45 positively affected the growth of soybean plants, making it a strong candidate for further studies on biofertilizer formulation.

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References

  1. Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B et al (2015) The extent of grain yield and plant growth enhancement by plant growth-promoting broad-spectrum Streptomyces sp. in chickpea. SpringerPlus 4:31

    PubMed  PubMed Central  Google Scholar 

  2. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39

    CAS  PubMed  Google Scholar 

  3. Palaniyandi SA, Damodharan K, Yang SH, Suh JW (2014) Streptomyces sp. strain PGPA39 alleviates salt stress and promotes growth of “Micro Tom” tomato plants. J Appl Microbiol 117:766–773

    CAS  PubMed  Google Scholar 

  4. Luo Q, Hu H, Peng H, Zhang X, Wang W (2015) Isolation and structural identification of two bioactive phenazines from Streptomyces griseoluteus P510. Chinese J Chem Eng 23:699–703

    CAS  Google Scholar 

  5. Mhlongo MI, Piater LA, Madala NE, Labuschagne N, Dubery IA (2018) The chemistry of plant–microbe interactions in the rhizosphere and the potential for metabolomics to reveal signaling related to defense priming and induced systemic resistance. Front Plant Sci 9:112. https://doi.org/10.3389/fpls.2018.00112

    Article  PubMed  PubMed Central  Google Scholar 

  6. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350

    CAS  PubMed  Google Scholar 

  7. Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microb Biochem Technol 7:96–102

    CAS  Google Scholar 

  8. Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecotoxicol Environm Saf 156:225–246

    CAS  Google Scholar 

  9. Bishnoi U (2015) PGPR interaction: an ecofriendly approach promoting the sustainable agriculture system. In: Advances in botanical research, vol 75. Academic Press, pp 81–113

  10. Wang Y, Luo Q, Zhang X, Wang W (2011) Isolation and purification of a modified phenazine, griseoluteic acid, produced by Streptomyces griseoluteus P510. Res Microbiol 162:311–319

    CAS  PubMed  Google Scholar 

  11. Dalmas FR, Pereira TCB, Bogo MR, Astarita LV (2011) Autochthonous Streptomyces regulate the metabolism of seedlings of Araucaria angustifolia (Coniferales) during root colonisation. Aust J Bot 59:118–125

    CAS  Google Scholar 

  12. Dias MP, Bastos MS, Xavier VB, Cassel E, Astarita LV, Santarém ER (2017) Plant growth and resistance promoted by Streptomyces spp. in tomato. Plant Physiol Biochem 118:479–493

    CAS  PubMed  Google Scholar 

  13. Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H (2012) Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28:1503–1509

    CAS  PubMed  Google Scholar 

  14. Salla TD, Ramos da Silva T, Astarita LV, Santarém ER (2014) Streptomyces rhizobacteria modulate the secondary metabolism of Eucalyptus plants. Plant Physiol Biochem 85:14–20

    CAS  PubMed  Google Scholar 

  15. Gong Y, Bai JL, Yang HT, Zhang WD, Xiong YW, Ding P, Qin S (2018) Phylogenetic diversity and investigation of plant growth-promoting traits of actinobacteria in coastal salt marsh plant rhizospheres from Jiangsu, China. Syst Appl Microbiol 41:516–527. https://doi.org/10.1016/j.syapm.2018.06.003

    Article  CAS  PubMed  Google Scholar 

  16. Mingma R, Pathom-aree W, Trakulnaleamsai S, Thamchaipenet A, Duangmal K (2014) Isolation of rhizospheric and roots endophytic actinomycetes from Leguminosae plant and their activities to inhibit soybean pathogen Xanthomonas campestris pv. glycine. World J Microbiol Biotechnol 30:271–280

    CAS  PubMed  Google Scholar 

  17. Drogue B, Doré H, Borland S, Wisniewski-Dyé F, Prigent-Combaret C (2012) Which specificity in cooperation between phytostimulating rhizobacteria and plants? Res Microbiol 163(8):500–510

    PubMed  Google Scholar 

  18. Nonomura H, Hayakawa M (1988) New methods for the selective isolation of soil actinomycets. In: Okami Y, Beppu T, Ogawara H (eds) Biology of actinomycetes 88: proceedings of seventh international symposium on biology of actinomycetes. Japan Scientific Societies Press, Tokyo, pp 288–293

    Google Scholar 

  19. Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Google Scholar 

  20. Dhanasekaran D, Jiang Y (2016) Actinobacteria—basics and biotechnological applications. IntechOpen, London, p 387

    Google Scholar 

  21. Dingle J, Reid WW, Solomons GL (1953) The enzymic degradation of pectin and other polysaccharides. II-Application of the ‘cup-plate’ assay to the estimation of enzymes. J Sci Food Agric 4:149–155

    CAS  Google Scholar 

  22. Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Sci Soc Am J 63:1670–1680

    CAS  Google Scholar 

  23. Dworkin M, Foster JW (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–603

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Salkowski E (1885) Ueber das verhalten der skatolcarbonsäure im organismus. Zeitschr Physiol Chem 9:23–33

    Google Scholar 

  25. Kadam MS, Patil SG, Dane PR, Pawar MK, Chincholkar SB (2013) Methods for purification and characterization of microbial phenazines. In: Microbial Phenazines. Springer, Berlin, Heidelberg, pp 101–140

    Google Scholar 

  26. Cezairliyan B, Vinayavekhin N, Grenfell-Lee D, Yuen GJ, Saghatelian A, Ausubel FM (2013) Identification of Pseudomonas aeruginosa phenazines that kill Caenorhabditis elegans. PLoS Pathog 9:e1003101

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Kern SE, Newman DK (2014) Measurement of phenazines in bacterial cultures. In: Filloux A, Ramos J-L (eds) Pseudomonas methods and protocols, vol 1149. Springer, New York, pp 303–310

    Google Scholar 

  28. Salla TD, Astarita LV, Santarém ER (2016) Defense responses in plants of Eucalyptus elicited by Streptomyces and challenged with Botrytis cinerea. Planta 243:1055–1070

    CAS  PubMed  Google Scholar 

  29. Tamreihao K, Ningthoujam DS, Nimaichand S, Singh ES, Reena P, Singh SH, Nongthomba U (2016) Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbiol Res 192:260–270

    CAS  PubMed  Google Scholar 

  30. Rey T, Dumas B (2017) Plenty is no plague: Streptomyces symbiosis with crops. Trends Plant Sci 22:30–37

    CAS  PubMed  Google Scholar 

  31. 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 

  32. Singh RP, Manchanda G, Maurya IK, Maheshwari NK, Tiwari PK, Rai AK (2019) Streptomyces from rotten wheat straw endowed the high plant growth potential traits and agro-active compounds. Biocatal Agricult Biotechn 17:507–513. https://doi.org/10.1016/j.bcab.2019.01.014

    Article  Google Scholar 

  33. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149

    CAS  PubMed  Google Scholar 

  34. Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97:9621–9636

    CAS  PubMed  Google Scholar 

  35. Egamberdieva D, Wirth SJ, Alqarawi AA, Abd Allah EF, Hashem A (2017) Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02104

  36. Gopalakrishnan S, Vadlamudi S, Bandikinda P, Sathya A, Vijayabharathi R, Rupela O, Kudapa H, Katta K, Varshney RK (2014) Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiol Res 169:40–48

    CAS  PubMed  Google Scholar 

  37. Mafia RG, Alfenas AC, Maffia LA, Ferreira EM, Binoti DHB, Mafia GMV (2009) Plant growth promoting rhizobacteria as agents in the biocontrol of eucalyptus mini-cutting rot. Trop Plant Pathol 34:10–17

    Google Scholar 

  38. Siddikee MA, Chauhan PS, Anandham R, Han G-H, Sa T (2010) Isolation, characterization, and use for plant growth promotion under salt stress of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584

    CAS  PubMed  Google Scholar 

  39. Jaemsaeng R, Jantasuriyarat C, Thamchaipenet A (2018) Molecular interaction of 1-aminocyclopropane-1-carboxylate deaminase (ACCD)-producing endophytic Streptomyces sp. GMKU 336 towards salt-stress resistance of Oryza sativa L. cv. KDML105. Sci Rep 8:1950

    PubMed  PubMed Central  Google Scholar 

  40. Pierson LS, Pierson EA (2010) Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol 86:1659–1670

    CAS  PubMed  PubMed Central  Google Scholar 

  41. de Vleesschauwer D, Cornelis P, Höfte M (2006) Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Mol Plant-Microbe Interact 19:1406–1419

    PubMed  Google Scholar 

  42. Xu S, Pan X, Luo J, Wu J, Zhou Z, Liang X, He Y, Zhou M (2015) Effects of phenazine-1-carboxylic acid on the biology of the plant-pathogenic bacterium Xanthomonas oryzae pv. oryzae. Pestic Biochem Physiol 117:39–46

    CAS  PubMed  Google Scholar 

  43. Das T, Ibugo AI, Klare W, Manefield M. Role of pyocyanin and extracellular DNA in facilitating Pseudomonas aeruginosa biofilm formation. In: Dhanasekaran D, Thajuddin N. Microbial biofilms—importance applications. IntechOpen; 2016. pp. 23–42

  44. Kasim WA, Gaafar RM, Abou-Ali RM, Omar MN, Hewait HM (2016) Effect of biofilm forming plant growth promoting rhizobacteria on salinity tolerance in barley. Ann Agricult Sci 61:217–227

    Google Scholar 

  45. Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18

    CAS  PubMed  Google Scholar 

  46. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15

    Google Scholar 

  47. Semêdo LTAS, Linhares AA, Gomes RC, Manfio GP, Alviano CS, Linhares LF, Coelho RRR (2001) Isolation and characterization of actinomycetes from Brazilian tropical soils. Microbiol Res 155:291–299

    PubMed  Google Scholar 

  48. Suela Silva M, Naves Sales A, Teixeira Magalhães-Guedes K, Ribeiro Dias D, Schwan RF (2013) Brazilian cerrado soil actinobacteria ecology. Biomed Res Int 2013:1–10

    Google Scholar 

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Acknowledgments

The authors thank Janaina Belquis da S. P. Langois and Rafaela Sole for their technical and laboratory assistance. The License for Research on Brazil’s Biodiversity was granted by the National Council for Scientific and Technological Development (CNPq 010539/2013-1).

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001, through fellowship of the first author and by the National Council for Scientific and Technological Development (CNPq/Brazil) through fellowship of the third author. Partial financial support was provided by CNPq/Brazil (403843/2013-8). In addition, this research was co-financed by Ballagro AgroTechnologia Ltda., São Paulo, Brazil (AGT/TA 01/2015-SIGPDI 194).

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Authors and Affiliations

  1. Escola de Ciências da Saúde e da Vida, Laboratório de Biotecnologia Vegetal, Pontifícia Universidade Católica do Rio Grande do Sul, Av. Ipiranga 6681, Porto Alegre, Rio Grande do Sul, 90619-900, Brazil

    Juliana Lopes Horstmann, Maila Pacheco Dias, Francieli Ortolan, Leandro Vieira Astarita & Eliane Romanato Santarém

  2. Escola de Ciências da Saúde e da Vida, Laboratório de Imunologia e Microbiologia, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, RS, Brazil

    Renata Medina-Silva

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  1. Juliana Lopes Horstmann
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Correspondence to Eliane Romanato Santarém.

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Horstmann, J.L., Dias, M.P., Ortolan, F. et al. Streptomyces sp. CLV45 from Fabaceae rhizosphere benefits growth of soybean plants. Braz J Microbiol 51, 1861–1871 (2020). https://doi.org/10.1007/s42770-020-00301-5

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