Advertisement

Vegetos

, Volume 32, Issue 1, pp 103–109 | Cite as

Stenotrophomonas: a versatile diazotrophic bacteria from the rhizospheric soils of Western Himalayas and development of its liquid biofertilizer formulation

  • Ajay KumarEmail author
  • Ruchi Soni
  • Sarbjit Singh Kanwar
  • Sunil Pabbi
Research Articles
  • 5 Downloads

Abstract

Rhizosphere is a rich repository of plant growth promoting rhizobacteria (PGPR) which is a sustainable tool to increase crop productivity and maintain soil health. In this context, 43 isolates were obtained on Jensen’s medium from the rhizosphere of Triticum aestivum, Zea mays, Solanum tuberosum, Aloe barbadensis and Bacopa monnieri grown in Palampur, (Himachal Pradesh) India. Out of these isolates, only six isolates (WT-A2, WT-A1, MZ-A2, PT-A1, PT-A3 and BM-A3) exhibited significantly higher nitrogenase activity (451.45, 441.58, 440.91, 444.02, 383.64 and 374.44 nmole C2H4 h−1 mg−1 protein) as compared to the reference strain of Azotobacter chroococum MTCC 446 (372.85 nmole C2H4 h−1 mg−1 protein). The isolate WT-A2 was the most efficient with respect to nitrogenase activity (451.45 nmole C2H4 h−1 mg−1 protein), indole acetic acid production (17.45 μg ml−1), ammonia production and siderophore production. Isolate WT-A2 was identified as Stenotrophomonas rhizophila on the basis of morphological, biochemical and 16S rRNA sequence analysis. In order to prepare liquid bioinoculant formulation, survivability studies on S. rhizophila was carried out in four different liquid carriers (Compost Tea, Biogas slurry, Vermiwash and Minimal Growth Medium) at room temperature (average maximum temp. was 23.83 °C and average minimum temp. was 11.91 °C). The results showed that S. rhizophila survived better in different liquid carriers (9.873 log cfu ml−1 in biogas slurry; 9.843 log cfu ml−1 in vermiwash; 9.163 log cfu ml−1 in minimal growth medium), and Compost Tea was the best carrier to support higher bacterial load (9.907 log cfu ml−1) on 180th day of storage. The results are of practical importance as this (compost tea) liquid carrier could be used to produce liquid biofertilizer formulation. Also, S. rhizophila could be a potential biofertilizer candidate as it posses multifarious plant growth promoting traits.

Keywords

Liquid carriers Nitrogenase PGPR, Rhizosphere 16S rRNA gene Stenotrophomonas rhizophila 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Uni-Sci 26:1–20.  https://doi.org/10.1016/j.jksus.2013.05.001 CrossRefGoogle Scholar
  2. Andrade G, Esteban E, Velascol L, Maria JL, Bedmar EJ (1997) Isolation and identification of N2-fixing microorganisms from the rhizosphere of Capparis spinosa (L.). Plant Soil 197:19–23.  https://doi.org/10.1023/A:1004211909641 CrossRefGoogle Scholar
  3. Asano Y, Lubbehusen TL (2000) Enzymes acting on peptides containing d-amino acid. J Biosci Bioeng 89:295–306.  https://doi.org/10.1016/S1389-1723(00)88949-5 CrossRefGoogle Scholar
  4. Bakker AW, Schippers P (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp.-mediated plant growth-stimulation. Soil Biol Biochem 19:451–457.  https://doi.org/10.1016/0038-0717(87)90037-X CrossRefGoogle Scholar
  5. Banerjee M, Yesmin L (2002) Sulfur-oxidizing plant growth promoting rhizobacteria for enhanced canola performance. US Patent 07491535Google Scholar
  6. Bashan Y (1998) Inoculants of plant growth-promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770.  https://doi.org/10.1016/S0734-9750(98)00003-2 CrossRefGoogle Scholar
  7. Basu S, Rabara RC, Negi S, Shukla P (2018) Engineering PGPMOs through gene editing and systems biology: a solution for phytoremediation? Trends Biotechnol 36:499–510.  https://doi.org/10.1016/j.tibtech.2018.01.011 CrossRefGoogle Scholar
  8. Benizri E, Courtade A, Picard C, Guckert A (1998) Role of maize root exudates in the production of auxins by Pseudomonas fluorescens M.3.1. Soil Biol Biochem 30:1481–1484.  https://doi.org/10.1016/S0038-0717(98)00006-6 CrossRefGoogle Scholar
  9. Blomberg A, Adler L (1992) Physiology of osmotolerance in fungi. Adv Microbial Physiol 33:145–212.  https://doi.org/10.1016/S0065-2911(08),60217-9 CrossRefGoogle Scholar
  10. Brown AD (1978) Compatible solutes and extreme water stress in eukaryotic microorganisms. Adv Microbial Physiol 17:181–242.  https://doi.org/10.1016/S0065-2911(08),60058-2 CrossRefGoogle Scholar
  11. Denet E, Vasselon V, Burdin B, Nazaret S, Favre-Bonte S (2018) Survival and growth of Stenotrophomonas maltophilia in free-living amoebae (FLA) and bacterial virulence properties. PLoS One 13(2):e0192308.  https://doi.org/10.1371/journal.pone.0192308 CrossRefGoogle Scholar
  12. Diver S (2003) Promoting biodynamic practices in Uttaranchal. Technical consultancy report submitted to Farmer-to-Farmer Program (USAID) Winrock International, USAGoogle Scholar
  13. Dubey KK, Fulekar MH (2013) Investigation of potential rhizospheric isolate for cypermethrin degradation. 3 Biotech 3:33–43.  https://doi.org/10.1007/s13205-012-0067-3 CrossRefGoogle Scholar
  14. Estenson K, Hurst GB, Standaert RF, Bible AN, Garcia D, Chourey K, Doktycz MJ, Morrell-Falvey JL (2018) Characterization of Indole-3-acetic Acid biosynthesis and the effects of this phytohormone on the proteome of the plant-associated microbe Pantoea sp. YR343. J Proteome Res 17:1361–1374CrossRefGoogle Scholar
  15. Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195.  https://doi.org/10.1104/pp.26.1.192 CrossRefGoogle Scholar
  16. Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140.  https://doi.org/10.1016/j.micres.2017.08.016 CrossRefGoogle Scholar
  17. Gulati A, Sood S, Rahi P, Thakur R, Chauhan S, Chadha IC (2011) Diversity analysis of diazotrophic bacteria associated with the roots of tea (Camellia sinensis (L.) O. Kuntze). J Microbiol Biotechnol 21:545–555.  https://doi.org/10.4014/jmb.1012.12022 Google Scholar
  18. Hardy RWF, Holsten RD, Jackson EK (1968) The acetylene-ethylene assay for N2-fixation-laboratory and field evaluation. Plant Physiol 43:118–127.  https://doi.org/10.1104/pp.43.8.1185 Google Scholar
  19. Heddi A, Charles H, Khatchadourian C, Bonnot G, Nardon P (1998) Molecular characterization of the principal symbiotic bacteria of the Weevil Sitophilus oryzae: a peculiar G + C content of an endocytobiotic DNA. J Mol Evol 47:52–61.  https://doi.org/10.1007/PL00006362 CrossRefGoogle Scholar
  20. Hegde SV (2008) Liquid biofertilizers in Indian agriculture. Biofertil Newslett 12:17–22Google Scholar
  21. Holt JG, Krieg RN, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology. 9. Williams and Wilkins, Baltimore, USAGoogle Scholar
  22. Igiehon NO, Babalola OO (2018) Rhizosphere microbiome modulators: contributions of nitrogen fixing bacteria towards sustainable agriculture. Int J Environ Res Public Health 15:574.  https://doi.org/10.3390/ijerph15040574 CrossRefGoogle Scholar
  23. Imam J, Singh PK, Shukla P (2016) Plant microbe interactions in post genomic era: perspectives and applications. Front Microbiol 7:1488.  https://doi.org/10.3389/fmicb.2016.01488 CrossRefGoogle Scholar
  24. Imam J, Shukla P, Prasad MN, Variar M (2017) Microbial interactions in plants: perspectives and applications of proteomics. Cur Protein Peptide Sci 18:956–965.  https://doi.org/10.2174/1389203718666161122103731 Google Scholar
  25. Karagoz K, Ates F, Karagoz H, Kotan R, Cakmakc R (2012) Characterization of plant growth-promoting traits of bacteria isolated from the rhizosphere of grapevine grown in alkaline and acidic soils. Eur J Soil Biol 50:144–150.  https://doi.org/10.1016/j.ejsobi.2012.01.007 CrossRefGoogle Scholar
  26. Kaur J, Pandove G, Gangwar M, Brar SK (2018) Development of liquid inoculants: an innovative agronomic practice for sustainable agriculture. J Exp Biol Agric Sci 6:472–481.  https://doi.org/10.18006/2018.6(3).472.481 Google Scholar
  27. Khan A, Singh P, Srivastava P (2018) Synthesis, nature and utility of universal iron chelator—siderophore: a review. Microbiol Res 212–213:103–111.  https://doi.org/10.1016/j.micres.2017.10.012 CrossRefGoogle Scholar
  28. Kumar A, Kumar A, Pratush A (2014) Molecular diversity and functional variability of environmental isolates of Bacillus species. SpringerPlus 3:312.  https://doi.org/10.1186/2193-1801-3-312 CrossRefGoogle Scholar
  29. Kumar S, Stecher G, Tamura K (2016a) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  30. Kumar V, Baweja M, Singh PK, Shukla P (2016b) Recent developments in systems biology and metabolic engineering of plant-microbe interactions. Front Plant Sci 7:1421.  https://doi.org/10.3389/fpls.2016.01421 Google Scholar
  31. Lorda G, Balatti A (1996) Designing media I and II. In: Balatti AP, Freire JRJ (eds) Legume inoculants, selection and characterization of strains, production, use and management. Kingraf, Buenos Aires, p 148Google Scholar
  32. Lowry OH, Rosebrough NJ, Farr AG, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275Google Scholar
  33. Mahanty T, Bhattacharjee S, Goswami M, Bhattacharyya P, Das B, Ghosh A, Tribedi P (2017) Biofertilizers: a potential approach for sustainable agriculture development. Environ Sci Pollut Res 24:3315.  https://doi.org/10.1007/s11356-016-8104-0 CrossRefGoogle Scholar
  34. Malusa E, Sas-Paszt L, Ciesielska J (2012) Technologies for beneficial microorganisms inocula used as biofertilizers. Sci World J 2012:491206.  https://doi.org/10.1100/2012/491206 CrossRefGoogle Scholar
  35. Marek-Kozaczuk M, Deryto M, Skorupska A (1996) Tn5 insertion mutants of Pseudomonas sp. 267 defective in siderophore production and their effect on clover (Trifolium pratense) nodulated with Rhizobium leguminosarum bv. trifollii. Plant Soil 179:269–274.  https://doi.org/10.1007/BF00009337 CrossRefGoogle Scholar
  36. Martinez-Hidalgo P, Maymon M, Pule-Meulenberg F, Hirsch AM (2019) Engineering root microbiomes for healthier crops and soils using beneficial, environmentally safe bacteria. Can J Microbiol 65:91–104.  https://doi.org/10.1139/cjm-2018-0315 CrossRefGoogle Scholar
  37. Mehnaz S, Weselowski B, Lazarovits G (2007) Azospirillum canadense sp. nov., a nitrogen-fixing bacterium isolated from corn rhizosphere. Int J Syst Evol Microbiol 57:620–624.  https://doi.org/10.1099/ijs.0.64804-0 CrossRefGoogle Scholar
  38. Park M, Kim C, Yang J, Lee H, Shin W, Kim S, Sa T (2005) Isolation and characterization of diazotrophic growth promoting bacteria from rhizosphere of agricultural crops of Korea. Microbiol Res 160:127–133.  https://doi.org/10.1016/j.micres.2004.10.003 CrossRefGoogle Scholar
  39. Parnell JJ, Berka R, Young HA, Sturino JM, Kang Y, Barnhart DM, DiLeo MV (2016) From the lab to the farm: an industrial perspective of plant beneficial microorganisms. Front Plant Sci 7:1110.  https://doi.org/10.3389/fpls.2016.01110 CrossRefGoogle Scholar
  40. Ramos PL, Moreira-Filho CA, Trappen SV, Swings J, Vos PD, Barbosa HR, Thompson CC, Vasconcelos ATR, Thompson FL (2011) An MLSA-based online scheme for the rapid identification of Stenotrophomonas isolates. Mem Inst Oswaldo Cruz 106:394–399.  https://doi.org/10.1590/S0074-02762011000400003 CrossRefGoogle Scholar
  41. Reinhardt EL, Ramos PL, Manfio GP, Barbosa HR, Pavan C, Moreira-Filho CA (2008) Molecular characterization of nitrogen-fixing bacteria isolated from Brazilian agricultural plants at Sao Paulo state. Braz J Microbiol 39:414–422.  https://doi.org/10.1590/S1517-83822008000300002 CrossRefGoogle Scholar
  42. Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van der Lelie D, Dow JM (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev 7:514–525.  https://doi.org/10.1038/nrmicro2163 Google Scholar
  43. Saraf M, Thakker A, Patel BV (2008) Biocontrol activity of different species of Pseudomonas against phytopathogenic fungi in vivo and in vitro conditions. Int J Biotechnol Biochem 4:223–232Google Scholar
  44. Saribay GF (2003) Growth and nitrogen fixation dynamics of Azotobacter chroococcum in nitrogen-free and OMW contaminating medium. M.Sc. Thesis, The Graduate School of Natural and Applied Sciences of the Middle East Technical UniversityGoogle Scholar
  45. Schwyn B, Neilands JB (1987) Universal chemical assay for detection and determination of siderophore. Anal Biochem 160:47–56.  https://doi.org/10.1016/0003-2697(87)90612-9 CrossRefGoogle Scholar
  46. Singh RP, Jha PN (2017) The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Front Microbiol 8:1945.  https://doi.org/10.3389/fmicb.2017.01945 CrossRefGoogle Scholar
  47. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448.  https://doi.org/10.1111/j.1574-6976.2007.00072.x CrossRefGoogle Scholar
  48. Sui J, Ji C, Wang X, Liu Z, Sa R, Hu Y, Wang C, Li Q, Liu X (2019) A plant-growth promoting bacterium alters the microbial community of continuous cropping poplar trees rhizosphere. J Appl Microbiol.  https://doi.org/10.1111/jam.14194 Google Scholar
  49. Sunder S, Singh AJ, Gill S, Singh B (1996) Regulation of intracellular level of Na+, K+ and glycerol in Saccharomyces cerevisiae under osmotic stress. Mol Cell Biochem 158:121–124.  https://doi.org/10.1007/BF00225837 CrossRefGoogle Scholar
  50. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680.  https://doi.org/10.1093/nar/22.22.4673 CrossRefGoogle Scholar
  51. Tkacz A, Poole P (2015) Role of root microbiota in plant productivity. J Exp Bot 66:2167–2175.  https://doi.org/10.1093/jxb/erv157 CrossRefGoogle Scholar
  52. Tsavkelova EA, Cherdyntseva TA, Botina SG, Netrusov AI (2007) Bacteria associated with orchid roots and microbial production of auxin. Microbiol Res 162:69–76.  https://doi.org/10.1016/j.micres.2006.07.014 CrossRefGoogle Scholar
  53. Tyagi S, Mulla SI, Lee KJ, Chae JC, Shukla P (2018) VOCs-mediated hormonal signaling and crosstalk with plant growth promoting microbes. Crit Rev Biotechnol 38:1277–1296.  https://doi.org/10.1080/07388551.2018.1472551 CrossRefGoogle Scholar
  54. Vejan P, Abdullah R, Khadiran T, Ismail S, Boyce AN (2018) Role of plant growth promoting rhizobacteria in agricultural sustainability-a review. Molecules 21:573.  https://doi.org/10.3390/molecules21050573 CrossRefGoogle Scholar
  55. Venieraki A, Dimou M, Pergalis P, Kefalogianni I, Chatzipavlidis I, Katinakis P (2011) The genetic diversity of culturable nitrogen-fixing bacteria in the rhizosphere of wheat. Microb Ecol 61:277–285.  https://doi.org/10.1007/s00248-010-9747-x CrossRefGoogle Scholar
  56. Verma M, Mishra J, Arora NK (2019) Plant growth-promoting rhizobacteria: diversity and applications. In: Sobti RC, Arora NK, Kothari R (eds) Environmental biotechnology: for sustainable future. Springer, Singapore, pp 129–173CrossRefGoogle Scholar
  57. Winkelmann G (1991) Specificity of iron transport in bacteria and fungi. In: Winkelmann G (ed) Handbook of microbial iron chelates. CRC Press, Boca Raton, pp 65–105Google Scholar

Copyright information

© Society for Plant Research 2019

Authors and Affiliations

  1. 1.Department of MicrobiologyCollege of Basic Sciences, CSK Himachal Pradesh Agricultural UniversityPalampurIndia
  2. 2.Department of Microbiology, School of Bioengineering and BiosciencesLovely Professional UniversityPhagwaraIndia
  3. 3.Division of Microbiology, National Centre for Conservation and Utilization of Blue Green AlgaeIARINew DelhiIndia

Personalised recommendations