Skip to main content
Log in

Differential effects of salinity and osmotic stress on the plant growth-promoting bacterium Gluconacetobacter diazotrophicus PAL5

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Plant growth-promoting bacteria (PGPB) represent a promising alternative to the massive use of industrial fertilizers in agriculture. Gluconacetobacter diazotrophicus is a PGPB that colonizes several plant species. Although this bacterium is able to grow at high sucrose concentrations, its response to environmental stresses is poorly understood. The present study evaluated G. diazotrophicus PAL5 response to stresses caused by sucrose, PEG 400, NaCl, KCl, Na2SO4 and K2SO4. Morphological, ultrastructural and cell growth analysis revealed that G. diazotrophicus PAL5 is more sensitive to salt than osmotic stress. Growth inhibition and strong morphological changes were caused by salinity, in consequence of Cl ion-specific toxic effect. Interestingly, low osmotic stress levels were beneficial for bacterial multiplication, which was able to tolerate high sucrose concentrations, Na2SO4 and K2SO4. Our data show that G. diazotrophicus PAL5 has differential response to osmotic and salinity stress, which may influence its use as inoculant in saline environments.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexander B, Leach S, Ingledew WJ (1987) The relationship between chemiosmotic parameters and sensitivity to anions and organic acids in the acidophile Thiobacillus ferrooxidans. J Gen Microbiol 133:1171–1179

    CAS  Google Scholar 

  • Baldani JI, Baldani VLD (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Cienc 77:549–579

    Article  CAS  PubMed  Google Scholar 

  • Boniolo FS, Rodrigues RC, Delatorre EO, da Silveira MM, Quintana Flores VM, Berbert-Molina MA (2009) Glycine betaine enhances growth of nitrogen-fixing bacteria Gluconacetobacter diazotrophicus PAL5 under saline stress conditions. Curr Microbiol 59:593–599. doi:10.1007/s00284-009-9479-7

    Article  CAS  PubMed  Google Scholar 

  • Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49:359–378

    CAS  PubMed  PubMed Central  Google Scholar 

  • Breedveld MW, Dijkema C, Zevenhuizen L, Zehnder AJB (1993) Response of intracellular carbohydrates to a NaCl shock in Rhizobium leguminosarum biovar trifolii TA-1 and Rhizobium meliloti SU-47. J Gen Microbiol 139:3157–3163

    Article  CAS  Google Scholar 

  • Brown AD (1964) Aspects of bacterial response to the ionic environment. Bacteriol Rev 28:296–329

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cavalcante V, Dobereiner J (1988) A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil 108:23–31. doi:10.1007/bf02370096

    Article  Google Scholar 

  • Chowdhury SP, Nagarajan T, Tripathi R, Mishra MN, Le Rudulier D, Tripathi AK (2007) Strain specific salt tolerance and osmoregulatory mechanisms in Azospirillum brasilense. FEMS Microbiol Lett 267:72–79

    Article  CAS  PubMed  Google Scholar 

  • Cocking EC, Stone PJ, Davey MR (2006) Intracellular colonization of roots of Arabidopsis and crop plants by Gluconacetobacter diazotrophicus. In Vitro Cell Dev Biol Plant 42:74–82

    Article  Google Scholar 

  • Cruz CD (2006) Programa genes—biometria, vol 1. Editora UFV, Viçosa

    Google Scholar 

  • DasSarma S, Arora P (2002) Halophiles. In: Encyclopedia of life sciences, vol 8. Nature Publishing Group, London, p 458–466

  • Deveci H, Jordan MA, Powell N, Alp I (2008) Effect of salinity and acidity on bioleaching activity of mesophilic and extremely thermophilic bacteria. Trans Nonferr Met Soc 18:714–721. doi:10.1016/s1003-6326(08)60123-5

    Article  CAS  Google Scholar 

  • Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2003) Physiological and community responses of established grassland bacterial populations to water stress. Appl Environ Microbiol 69:6961–6968. doi:10.1128/aem.69.12.6961-6968.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IFA (2013) International fertilizer industry association. http://www.fertilizer.org/ifa/ifadata/search. Accessed 03 June 2014

  • Intorne A, Oliveira M, Lima M, da Silva J, Fb Olivares, Gar Souza Filho (2009) Identification and characterization of Gluconacetobacter diazotrophicus mutants defective in the solubilization of phosphorus and zinc. Arch Microbiol 191:477–483. doi:10.1007/s00203-009-0472-0

    Article  CAS  PubMed  Google Scholar 

  • Koch S, Oberson G, Eugster-Meier E, Melle L, Lacroix C (2007) Osmotic stress induced by salt increases cell yield, autolytic activity, and survival of lyophilization of Lactobacillus delbrueckii subsp lactis. Int J Food Microbiol 117:36–42. doi:10.1016/j.ijfoodmicro.2007.01.016

    Article  CAS  PubMed  Google Scholar 

  • Krulwich TA, Sachs G, Padan E (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 9:330–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kucuk C, Kivanc M (2008) Preliminary characterization of Rhizobium strains isolated from chickpea nodules. Afr J Biotechnol 7:772–775. doi:10.5897/AJB08.026

    Google Scholar 

  • Lourdes Velazquez-Hernandez M et al (2011) Gluconacetobacter diazotrophicus levansucrase is involved in tolerance to NaCl, sucrose and desiccation, and in biofilm formation. Arch Microbiol 193:137–149. doi:10.1007/s00203-010-0651-z

    Article  PubMed  Google Scholar 

  • Luna MF, Galar ML, Aprea J, Molinari ML, Boiardi JL (2010) Colonization of sorghum and wheat by seed inoculation with G. diazotrophicus. Biotechnol Lett 32:1071–1076. doi:10.1007/s10529-010-0256-2

    Article  CAS  PubMed  Google Scholar 

  • Luna MF, Aprea J, Crespo JM, Boiardi JL (2011) Colonization and yield promotion of tomato by G. diazotrophicus. Appl Soil Ecol. doi:10.1016/j.apsoil.2011.09.002

    Google Scholar 

  • Madhaiyan A, Poonguzhali S, Hari K, Saravanan VS, Sa T (2006) Influence of pesticides on the growth rate and plant-growth promoting traits of G. diazotrophicus. Pestic Biochem Physiol 84:143–154. doi:10.1016/j.pestbp.2005.06.004

    Article  CAS  Google Scholar 

  • Miller KJ, Wood JM (1996) Osmoadaptation by rhizosphere bacteria. Annu Rev Microbiol 50:101–136. doi:10.1146/annurev.micro.50.1.101

    Article  CAS  PubMed  Google Scholar 

  • Moradi A, Tahmourespour A, Hoodaji M, Khorsandi F (2011) Effect of salinity on free living—diazotroph and total bacterial populations of two saline soils. Afr J Microbiol Res 5:144–148

    CAS  Google Scholar 

  • Muthukumarasamy R, Revathi G, Loganathan P (2002) Effect of inorganic N on the population, in vitro colonization and morphology of Acetobacter diazotrophicus (syn. G. diazotrophicus). Plant Soil 243:91–102. doi:10.1023/a:1019963928947

    Article  CAS  Google Scholar 

  • Oktyabrskii ON, Smirnova GV (2012) Redox potential changes in bacterial cultures under stress conditions. Microbiology 81:131–142. doi:10.1134/s0026261712020099

    Article  CAS  Google Scholar 

  • Pianetti A, Battistelli M, Citterio B, Parlani C, Falcieri E, Bruscolini F (2009) Morphological changes of Aeromonas hydrophila in response to osmotic stress. Micron 40:426–433

    Article  CAS  PubMed  Google Scholar 

  • Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443

    Article  PubMed  Google Scholar 

  • Rodrigues Neto J, Malavolta VA, Victor O (1986) Meio simples para o isolamento e cultivo de Xanthomonas campestris pv. citri tipo B. Summa Phytopathol 12:16

    Google Scholar 

  • Saravanan et al (2007) Zinc metal solubilization by G. diazotrophicus and induction of pleomorphic cells. J Microbiol Biotechnol 17:1477–1482

    CAS  PubMed  Google Scholar 

  • Saravanan VS, Madhaiyan M, Osborne J, Thangaraju M, Sa TM (2008) Ecological occurrence of Gluconacetobacter diazotrophicus and nitrogen-fixing Acetobacteraceae members: their possible role in plant growth promotion. Microb Ecol 55:130–140. doi:10.1007/s00248-007-9258-6

    Article  CAS  PubMed  Google Scholar 

  • Severin I, Confurius-Guns V, Stal L (2012) Effect of salinity on nitrogenase activity and composition of the active diazotrophic community in intertidal microbial mats. Arch Microbiol 194:483–491. doi:10.1007/s00203-011-0787-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shabala L, Bowman J, Brown J, Ross T, McMeekin T, Shabala S (2009) Ion transport and osmotic adjustment in Escherichia coli in response to ionic and non-ionic osmotica. Environ Microbiol 11:137–148. doi:10.1111/j.1462-2920.2008.01748.x

    Article  CAS  PubMed  Google Scholar 

  • Shi B, Xia X (2003) Morphological changes of Pseudomonas pseudoalcaligenes in response to temperature selection. Curr Microbiol 46:120–123

    Article  CAS  PubMed  Google Scholar 

  • Shiers DW, Blight KR, Ralph DE (2005) Sodium sulphate and sodium chloride effects on batch culture of iron oxidising bacteria. Hydrometallurgy 80:75–82

    Article  CAS  Google Scholar 

  • Sugawara M, Cytryn EJ, Sadowsky MJ (2010) Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol 76:1071–1081. doi:10.1128/aem.02483-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tejera NA, Ortega E, González López J, Lluch C (2003) Effect of some abiotic factors on the biological activity of Gluconacetobacter diazotrophicus. J Appl Microbiol 95:528–535

    Article  CAS  PubMed  Google Scholar 

  • van den Bogaart G, Hermans N, Krasnikov V, Poolman B (2007) Protein mobility and diffusive barriers in Escherichia coli: consequences of osmotic stress. Mol Microbiol 64:858–871. doi:10.1111/j.1365-2958.2007.05705.x

    Article  PubMed  Google Scholar 

  • Von Blottnitz H, Rabl A, Boiadjiev D, Taylor T, Arnold S (2006) Damage costs of nitrogen fertilizer in Europe and their internalization. J Environ Plann Man 49:413–433. doi:10.1080/09640560600601587

    Article  Google Scholar 

  • Wainwright M, Canham LT, Al-Wajeeh K, Reeves CL (1999) Morphological changes (including filamentation) in Escherichia coli grown under starvation conditions on silicon wafers and other surfaces. Lett Appl Microbiol 29:224–227

    Article  CAS  PubMed  Google Scholar 

  • Wood JM (2011) Bacterial osmoregulation: a paradigm for the study of cellular homeostasis. Annu Rev Microbiol 65:215–238. doi:10.1146/annurev-micro-090110-102815

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Jiang J, Wei W, Zhang B, Wang L, Yang S (2006) The pha2 gene cluster involved in Na+ resistance and adaption to alkaline pH in Sinorhizobium fredii RT19 encodes a monovalent cation/proton antiporter. FEMS Microbiol Lett 262:172–177. doi:10.1111/j.1574-6968.2006.00385.x

    Article  CAS  PubMed  Google Scholar 

  • Yang W, W-q Qin, R-q Liu, Y-c Ren (2011) Effect of chloride ion on bacterial pre-oxidation of arsenic-containing gold concentrate. J Cent South Univ T 18:1418–1424. doi:10.1007/s11771-011-0856-6

    Article  CAS  Google Scholar 

  • Zammit CM, Mangold S, Rao Jonna V, Mutch LA, Watling HR, Dopson M, Watkin ELJ (2012) Bioleaching in brackish waters-effect of chloride ions on the acidophile population and proteomes of model species. Appl Microbiol Biotechnol 93:319–329

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We want to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Financiadora de Estudos e Projetos (FINEP), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Instituto Nacional de Ciência e Tecnologia da Fixação Biológica de Nitrogênio (INCT-FBN), which have supported this research. The first author received a CAPES fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gonçalo A. De Souza Filho.

Ethics declarations

Competing interests

None declared.

Additional information

Communicated by Erko Stackebrandt.

Marcos Vinicius V. De Oliveira, Aline C. Intorne and Luciano de S. Vespoli have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

De Oliveira, M.V.V., Intorne, A.C., Vespoli, L.S. et al. Differential effects of salinity and osmotic stress on the plant growth-promoting bacterium Gluconacetobacter diazotrophicus PAL5. Arch Microbiol 198, 287–294 (2016). https://doi.org/10.1007/s00203-015-1176-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-015-1176-2

Keywords

Navigation