Skip to main content
SpringerLink
Log in

Choline–betaine pathway contributes to hyperosmotic stress and subsequent lethal stress resistance in Pseudomonas protegens SN15-2

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Pseudomonas protegens SN15-2, a typical non-spore-forming rhizosphere bacterium, has excellent biocontrol capabilities; thus, it is necessary to explore the stress resistance of SN15-2. The choline–glycine betaine pathway is considered as an important mechanism by which bacteria adapt to stressful environments. In this work, we demonstrated that the expression of the betA and betB genes, which are involved in the choline–glycine betaine pathway in SN15-2, was highly increased by 12-fold and 26-fold, respectively, by hyperosmotic stress and choline treatment. The accumulation of betaine in SN15-2 (5.54 g/L) was significantly higher than that in the mutants Δ betA (3.44 g/L) and Δ betB (2.68 g/L) under hyperosmotic stress and choline treatment. Moreover, choline enhanced the growth of SN15-2 greatly, but it did not enhance the growth of Δ betB under hyperosmotic stress. Choline combined with hyperosmotic adaptation significantly increased the lethal stress resistance of SN15-2 while the resistance of Δ betA and Δ betB was significantly decreased. This research illuminated a strategy underlying the adaptation to osmotic stress in P. protegens and provided an effective method to improve the stress resistance of this species, thus provided a theoretical basis for the practical application of P. protegens SN15-2.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  • Anderson WA, Hedges ND, Jones MV and Cole MB 1991 Thermal inactivation of Listeria monocytogenes studied by differential scanning calorimetry. J. Gen. Microbiol. 137 1419–1424

    Article  CAS  Google Scholar 

  • Barbosa J, Borges S and Teixeira P 2015 Influence of sub-lethal stresses on the survival of lactic acid bacteria after spray-drying in orange juice. Food Microbiol. 52 77–83

    Article  CAS  Google Scholar 

  • Beattie GA, Chen C, Nielsen L and Freeman BC 2016 Interstrain variation in the physiological and transcriptional responses of Pseudomonas syringae to osmotic stress; in Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria (eds) J Frans and D Bruijn (John Wiley & Sons, Inc) pp 647–656

  • Biryukova EN, Medentsev AG, Arinbasarova AY and Akimenko VK 2007 Adaptation of the yeast Yarrowia lipolyticato to heat shock. Microbiology 76 158–163

    Article  CAS  Google Scholar 

  • Boch J, Kempf B and Bremer E 1994 Osmoregulation in Bacillus subtilis: synthesis of the osmoprotectant glycine betaine from exogenously provided choline. J. Bacteriol. 176 5364–5371

    Article  CAS  Google Scholar 

  • Cabrefiga J, Francés J, Montesinos E and Bonaterra A 2014 Improvement of a dry formulation of Pseudomonas fluorescens EPS62e for fire blight disease biocontrol by combination of culture osmoadaptation with a freeze-drying lyoprotectant. J. Appl. Microbiol. 117 1122–1131

    Article  CAS  Google Scholar 

  • Chen C and Beattie GA 2007 Characterization of the osmoprotectant transporter OpuC from Pseudomonas syringae and demonstration that cystathionine-beta-synthase domains are required for its osmoregulatory function. J. Bacteriol. 189 6901–6912

    Article  CAS  Google Scholar 

  • Chen J, Wang X, Tang D and Wang W 2019 Oxidative stress adaptation improves the heat tolerance of Pseudomonas fluorescens SN15-2. Biol. Control 138 104070

    Article  CAS  Google Scholar 

  • Chen TH and Murata N 2011 Glycine betaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ. 34 1–20

    Article  Google Scholar 

  • Cheng Z, Chi M, Li G, Chen H, Sui Y, Sun H, Wisniewski M, Liu Y et al. 2016 Heat shock improves stress tolerance and biocontrol performance of Rhodotorula mucilaginosa. Biol. Control 95 49–56

    Article  CAS  Google Scholar 

  • Dunlap CA, Evans KO, Bart T, Teun B and Schisler DA 2007 Osmotic shock tolerance and membrane fluidity of cold-adapted Cryptococcus flavescens OH 182.9, previously reported as C. nodaensis, a biocontrol agent of Fusarium head blight. FEMS Yeast Res. 7 449–458

    Article  CAS  Google Scholar 

  • Frohlich A, Buddrus-Schiemann K, Durner J, Hartmann A and von Rad U 2012 Response of barley to root colonization by Pseudomonas sp. DSMZ 13134 under laboratory, greenhouse, and field conditions. J. Plant Interact. 7 1–9

    Article  Google Scholar 

  • Fu Q, Liu C, Ding N, Lin Y and Guo B 2010 Ameliorative effects of inoculation with the plant growth-promoting rhizobacterium Pseudomonas sp. DW1 on growth of eggplant (Solanum melongena L.) seedlings under salt stress. Agric. Water Manag. 97 1994–2000

    Article  Google Scholar 

  • Galinski EA and Trüper HG 1994 Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol. Rev. 15 95–108

    Article  CAS  Google Scholar 

  • Galvão TC, De Lorenzo V and Cánovas D 2006 Uncoupling of choline -O- sulphate utilization from osmoprotection in Pseudomonas putida. Mol. Microbiol. 62 1643–1654

    Article  Google Scholar 

  • Guan N, Li J, Shin H-d, Du G, Chen J and Liu L 2017 Microbial response to environmental stresses: from fundamental mechanisms to practical applications. Appl. Microbiol. Biotechnol. 101 3991–4008

    Article  CAS  Google Scholar 

  • Haas D and Defago G 2005 Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat. Rev. Microbiol. 3 307–319

    Article  CAS  Google Scholar 

  • Huang W and Wilks A 2017 A rapid seamless method for gene knockout in Pseudomonas aeruginosa. BMC Microbiol. 17 1–8

    Article  Google Scholar 

  • Kempf B and Bremer E 1998 Stress responses of Bacillus subtilis to high osmolarity environments: Uptake and synthesis of osmoprotectants. J. Biosci. 23 447–455

    Article  CAS  Google Scholar 

  • Kets EPW, de Bont JAM and Heipieper HJ 1996 Physiological response of Pseudomonas putida S12 subjected to reduced water activity. FEMS Microbiol. Lett. 139 133–137

    Article  CAS  Google Scholar 

  • Koga T, Katagiri T, Hori H and Takumi K 2002 Alkaline adaptation induces cross-protection against some environmental stresses and morphological change in Vibrio parahaemolyticus. Microbiol. Res. 157 249–255

    Article  Google Scholar 

  • Koga T and Takumi K 1995 Nutrient starvation induces cross protection against heat, osmotic, or H2O2 challenge in Vibrio parahaemolyticus. Microbiol. Immunol. 39 213–215

    Article  CAS  Google Scholar 

  • Lamark T, Kaasen I, Eshoo MW, Falkenberg P, McDougall J and Strom AR 1991 DNA sequence and analysis of the bet genes encoding the osmoregulatory choline—glycine betaine pathway of Escherichia coli. Mol. Microbiol. 5 1049–1064

    Article  CAS  Google Scholar 

  • Landfald B and Strm AR 1986 Choline–glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J. Bacteriol. 165 849–855

    Article  CAS  Google Scholar 

  • Rudulier DL, Strom AR, Dandekar A, Smith L and Valentine R 1984 Molecular biology of osmoregulation. Science 224 1064–1068

    Article  Google Scholar 

  • Li X, Gu G, Chen W, Gao L, Wu X and Zhang L 2018 The outer membrane protein OprF and the sigma factor SigX regulate antibiotic production in Pseudomonas fluorescens 2P24. Microbiol. Res. 206 159–167

    Article  CAS  Google Scholar 

  • Liu J, Wisniewski M, Droby S, Norelli J, Hershkovitz V, Tia S and Farrell R 2012 Increase in antioxidant gene transcripts, stress tolerance and biocontrol efficacy of Candida oleophila following sublethal oxidative stress exposure. FEMS Microbiol. Ecol. 80 578–590

    Article  CAS  Google Scholar 

  • Lou H, Wang X, Chen J, Wang B and Wang W 2018 Transcriptomic response of Ralstonia solanacearum to antimicrobial Pseudomonas fluorescens SN15-2 metabolites. Can. J. Microbiol. 64 816–825

    Article  CAS  Google Scholar 

  • Lugtenberg B and Kamilova F 2009 Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63 541–556

    Article  CAS  Google Scholar 

  • Ma Y, Wang Q, Gao X and Zhang Y 2017 Biosynthesis and uptake of glycine betaine as cold-stress response to low temperature in fish pathogen Vibrio anguillarum. J. Microbiol. 55 44–55

    Article  CAS  Google Scholar 

  • Rodríguez-González O, Walkling-Ribeiro M, Jayaram S and Griffiths MW 2011 Cross-protective effects of temperature, pH, and osmotic and starvation stresses in Escherichia coli O157: H7 subjected to pulsed electric fields in milk. Int. Dairy J. 21 953–962

    Article  Google Scholar 

  • Sage AE, Vasil AI and Vasil ML 1997 Molecular characterization of mutants affected in the osmoprotectant-dependent induction of phospholipase C in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 23 43–56

    Article  CAS  Google Scholar 

  • Sand M, Stahl J, Waclawska I, Ziegler C and Averhoff B 2014 Identification of an osmo-dependent and an osmo-independent choline transporter in Acinetobacter baylyi: implications in osmostress protection and metabolic adaptation. Environ. Microbiol. 16 1490–1502

    Article  CAS  Google Scholar 

  • Velasco-García R, Mújica-Jiménez C, Mendoza-Hernández G and Muñoz-Clares RA 1999 Rapid purification and properties of betaine aldehyde dehydrogenase from Pseudomonas aeruginosa. J. Bacteriol. 181 1292–1300

    Article  Google Scholar 

  • Velasco-García R, Villalobos MA, Ramírez-Romero MA, Mujica-Jimenez C, Iturriaga G and Munoz-Clares RA 2006 Betaine aldehyde dehydrogenase from Pseudomonas aeruginosa: cloning, over-expression in Escherichia coli, and regulation by choline and salt. Arch. Microbiol. 185 14–22

    Article  Google Scholar 

  • Vyrides I and Stuckey DC 2017 Compatible solute addition to biological systems treating waste/wastewater to counteract osmotic and other environmental stresses: a review. Crit. Rev. Biotechnol. 37 865–879

    Article  CAS  Google Scholar 

  • Wang Y, Wang P, Xia J, Yu T, Lou B, Wang J and Zheng X 2010 Effect of water activity on stress tolerance and biocontrol activity in antagonistic yeast Rhodosporidium paludigenum. Int. J. Food Microbiol. 143 103–108

    Article  CAS  Google Scholar 

  • Wargo MJ 2013 Choline catabolism to glycine betaine contributes to Pseudomonas aeruginosa survival during murine lung infection. PLoS One 8 e56850

    Article  CAS  Google Scholar 

  • Wargo MJ and Matthew J 2013 Homeostasis and catabolism of choline and glycine betaine: lessons from Pseudomonas aeruginosa. Appl. Environ. Microbiol. 79 2112–2120

    Article  CAS  Google Scholar 

  • Whatmore AM and Reed RH 1990 Determination of turgor pressure in Bacillus subtilis: a possible role for K+ in turgor regulation. J. Gen. Microbiol. 136 2521–2526

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Key Research and Development Program of China under Grant number 2017YFD0200400; the Project of Prospering Agriculture through Science and Technology of Shanghai, China under Grant number Hu NongKeChuangZi (2018) No. 2–5.

Author information

Authors and Affiliations

  1. State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai, 200237, China

    Danyan Tang, Xiaobing Wang, Jian Wang, Mengfei Wang, Yaping Wang & Wei Wang

Authors
  1. Danyan Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaobing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mengfei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wei Wang.

Additional information

Communicated by Ashis Kumar Nandi.

Corresponding editor: Ashis Kumar Nandi

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tang, D., Wang, X., Wang, J. et al. Choline–betaine pathway contributes to hyperosmotic stress and subsequent lethal stress resistance in Pseudomonas protegens SN15-2. J Biosci 45, 85 (2020). https://doi.org/10.1007/s12038-020-00060-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12038-020-00060-3

Keywords

Search

Navigation