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Salt Tolerance Mechanism and Species Identification of the Plant Rhizosphere Bacterium JYZ-SD2

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Abstract

A salt-tolerant microbe strain JYZ-SD2 was investigated to develop biological soil amendments to stimulate salix growth and acclimation in costal salt-affected soils. The salt tolerance mechanism of strain JYZ-SD2 was investigated by detecting the salt-tolerant growth characteristics, biofilm formation, ion distribution, secondary metabolites, and zymogram profiling. The strain was identified by physiological and biochemical characteristics (Biolog), 16S rDNA sequencing, and cry1/7/9 gene expressing. With increasing of NaCl concentration, strain JYZ-SD2 adapted to the increased osmotic pressure by prolonging the retardation period, slowing down the growth rate of the logarithmic phase, increasing spo0A gene expression, increasing biofilm formation, reducing Na+ uptake, and changing the expression of metabolites and intracellular soluble proteins. The results showed that strain JYZ-SD2 could be assigned to Bacillus cereus.

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References

  1. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59(1):651–681

    Article  CAS  Google Scholar 

  2. Nusrat N, Shahbaz M, Perveen S (2014) Modulation in growth, photosynthetic efficiency, activity of antioxidants and mineral ions by foliar application of glycine betaine on pea (Pisum sativum L.) under salt stress. Acta Physiol Plant 36(11):2985–2998

    Article  CAS  Google Scholar 

  3. Mishra S, Upadhyay S, Shukla RK (2017) The role of strigolactones and their potential cross-talk under hostile ecological conditions in plants. Front Physiol 7:691

    Article  Google Scholar 

  4. Ahmad AF, Iqbal A (2018) Plant growth promoting attributes and alleviation of salinity stress to wheat by biofilm forming, Brevibacterium sp. FAB3 isolated from rhizospheric soil. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2018.08.003

    Article  PubMed  PubMed Central  Google Scholar 

  5. Vaidya S, Dev K, Sourirajan A (2018) Distinct osmoadaptation strategies in the strict halophilic and halotolerant bacteria isolated from lunsu salt water body of north west Himalayas. Curr Microbiol 75(7):888–895

    Article  CAS  Google Scholar 

  6. Saum SH, Volker M (2010) Growth phase-dependent switch in osmolyte strategy in a moderate halophile:ectoine is a minor osmolyte but major stationary phase solute in Halobacillus halophilus. Environ Microbiol 10(3):716–726

    Article  Google Scholar 

  7. Ivey DM, Guffanti AA, Bossewitch JS, Padan E, Krulwich TA (1991) Molecular cloning and sequencing of a gene from alkaliphilic Bacillus firmus OF4 that functionally complements an Escherichia coli strain carrying a deletion in the nhaA Na+/H+ antiporter gene. J Biol Chem 266(34):23483

    CAS  PubMed  Google Scholar 

  8. Jiang J, Wang L, Zou Y, Lu W, Zhao B, Zhang B et al (1828) (2013) Identification of important charged residues for alkali cation exchange or pH regulation of NhaH, a Na+/H+ antiporter of Halobacillus dabanensis. BBA-Biomembranes 3:997–1003

    Google Scholar 

  9. Ritika K, Gupta MK, Kumar N, Kanwar S (2017) Analysis of nhaA gene from salt tolerant and plant growth promoting Enterobacter ludwigii. Rhizosphere. https://doi.org/10.1016/j.rhisph.2017.07.002

    Article  Google Scholar 

  10. Wei X, Fang L, Cai P, Huang Q, Chen H, Liang W et al (2011) Influence of extracellular polymeric substances (EPS) on Cd adsorption by bacteria. Environ Pollut 159(5):1369–1374

    Article  CAS  Google Scholar 

  11. 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. J Agric Sci Cambridge 61:217–227

    Google Scholar 

  12. Dimkpa C, Weinand T, Asch F (2010) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32(12):1682–1694

    Article  Google Scholar 

  13. Castelijn GAA, Stijn VDV, Zwietering MH, Moezelaar R, Abee T (2012) Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella, typhimurium strains of different origin in high and low nutrient medium. Biofouling 28(1):51–63

    Article  CAS  Google Scholar 

  14. Gao T, Foulston L, Chai Y, Wang Q, Losick R (2015) Alternative modes of biofilm formation by plant-associated Bacillus cereus. Microbiology Open 4(3):452–464

    Article  CAS  Google Scholar 

  15. Lucking G, Dommel MK, Scherer S, Fouet A, Ehling-Schulz M (2009) Cereulide synthesis in emetic Bacillus cereus is controlled by the transition state regulator abrb, but not by the virulence regulator plcr. Microbiology 155(3):922–931

    Article  Google Scholar 

  16. Buchanan RE, Gibbons NE (1974) Bergey’s manual of determinative bacteriology, 8th edn. The William & Wilkins, Baltimore, pp 729–759

    Google Scholar 

  17. Li GE, Wu XQ, Ye J-R (2013) Isolation and identification of phytate-degrading rhizobacteria with activity of improving growth of poplar and masson pine. World J Microb Biotechnol 29(11):2181–2193

    Article  CAS  Google Scholar 

  18. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74(8):2461–2470

    Article  CAS  Google Scholar 

  19. Kuo WS, Chak KF (1996) Identification of novel cry-type genes from Bacillus thuringiensis strains on the basis of restriction fragment length polymorphism of the PCR-amplified DNA. Appl Environ Microbiol 62(4):1369–1377

    Article  CAS  Google Scholar 

  20. Zeng Q, Wu X, Wen X (2016) Identification and characterization of the rhizosphere phosphate-solubilizing bacterium Peudomonas frederiksbergensis JW-SD2, and its plant growth-promoting effects on poplar seedlings. Ann Microbiol 66(4):1343–1354

    Article  CAS  Google Scholar 

  21. Sadeghi A, Soltani BM, Nekouei MK, Jouzani GS, Mirzaei HH, Sadeghizadeh M (2014) Diversity of the ectoines biosynthesis genes in the salt tolerant streptomyces and evidence for inductive effect of ectoines on their accumulation. Microbiol Res 169(9–10):699–708

    Article  CAS  Google Scholar 

  22. Shivanand P, Mugeraya G (2011) Halophilic bacteria and their compatible solutes—osmoregulation and potential applications. Curr Sci India 100(10):25–2011

    Google Scholar 

  23. Dow JM, Ryan P (2008) Diffusible signals and interspecies communication in bacteria. Microbiology 154(7):1845

    Article  Google Scholar 

  24. Morikawa M (2006) Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. J Biosci Bioeng 101(1):1–8

    Article  CAS  Google Scholar 

  25. Zeng Q, Wu X, Wen X (2016) Effects of soluble phosphate on phosphate-solubilizing characteristics and expression of gcd gene in Pseudomonas frederiksbergensis JW-SD2. Curr Microbiol 72(2):198–206

    Article  CAS  Google Scholar 

  26. Park EJ, Hussain MS, Wei S, Kwon M (2019) Genotypic and phenotypic characteristics of biofilm formation of emetic toxin producing Bacillus cereus strains. Food Control 96:527–534

    Article  CAS  Google Scholar 

  27. Widderich N, Rodrigues C, Commichau F, Fischer K, Ramirez-Guadiana FH, Rudner DZ et al (2016) Salt-sensitivity of σH and Spo0A prevents sporulation of Bacillus subtilis at high osmolarity avoiding death during cellular differentiation. Mol Microbiol. 100(1):108–124

    Article  CAS  Google Scholar 

  28. Waheed QA, Nasim SA (2012) Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 43(3):1183–1191

    Article  Google Scholar 

  29. Li J, Xu H, Chen X, Xu L, Cheng R, Zhang J et al (2017) Characterization of an exopolysaccharide with distinct rheological properties from, Paenibacillus edaphicusnust16. Int J Biol Macromol 105(1):1–8

    Article  Google Scholar 

  30. Kaluzhnaya M, Khmelenina V, Eshinimaev B, Suzina N, Nikitin D, Solonin A et al (2001) Taxonomic characterization of new alkaliphilic and alkalitolerant methanotrophs from soda lakes of the southeastern transbaikal region and description of Methylomicrobium buryatense sp nov. Syst Appl Microbiol 24(2):166–176

    Article  CAS  Google Scholar 

  31. Taketo K, Soichi F, Naoki N, Chisato H et al (2009) Biofilm formation by Escherichia coli in hypertonic sucrose media. J Biosci Bioeng 107(6):630–635

    Article  Google Scholar 

  32. Southworth TW, Guffanti AA, Moir A, Krulwich TA (2001) Gern, an endospore germination protein of Bacillus cereus, is an Na+/H+-K+ antiporter. J Bacteriol 183(20):5896–5903

    Article  CAS  Google Scholar 

  33. Roeßler M, Müller V (1998) Quantitative and physiological analyses of chloride dependence of growth of Halobacillus halophilus. Appl Environ Microbiol 64(10):3813

    Article  Google Scholar 

  34. Chen Z, Pan X, Chen H, Guan X, Lin Z (2015) Biomineralization of pb(ii) into pb-hydroxyapatite induced by Bacillus cereus 12–2 isolated from lead-zinc mine tailings. J Hazardous Mater 301:531–537

    Article  Google Scholar 

  35. Karunakaran E, Biggs CA (2011) Mechanisms of Bacillus cereus biofilm formation: an investigation of the physicochemical characteristics of cell surfaces and extracellular proteins. Appl Microbiol Biotechnol 89(4):1161–1175

    Article  CAS  Google Scholar 

  36. Fang H, Hu B, Nie Y, Tang YQ, Wu XL (2017) The complete genome of Dietzia timorensis id05-a0528(t) revealed the genetic basis for its saline-alkali tolerance. J Biotechnol 241:11–13

    Article  CAS  Google Scholar 

  37. Lu W, Zhang B, Zhao B et al (2007) Cloning and characterization of the genes encoding a glycine betaine ABC-type transporter in Halobacillus trueperi DSM10404T. Curr Microbiol 54(2):124–130

    Article  CAS  Google Scholar 

  38. Li FY, Ju QJ, Bai SZ, Bo Z (2006) A Na+/H+ antiporter gene of the moderately halophilic bacterium Halobacillus dabanensis D-8T. FEMS Microbiol Lett 255(1):89–95

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Key Research and Development Program of China (Grant No. 2017YFD0600100) and the Priority Academic Development Program of Jiangsu Universities (PAPD). I am grateful to Dr. Prof. Eric C. Brevik, Dickinson State University, for his kind improving this paper.

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Wu, Ty., Wu, XQ., Xu, Xq. et al. Salt Tolerance Mechanism and Species Identification of the Plant Rhizosphere Bacterium JYZ-SD2. Curr Microbiol 77, 388–395 (2020). https://doi.org/10.1007/s00284-019-01835-0

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