Skip to main content
SpringerLink
Log in

Aqueous peat extract exposes rhizobia to sub-lethal stress which may prime cells for improved desiccation tolerance

  • Genomics, transcriptomics, proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Inoculation of legume seed with rhizobia is an efficient and cost-effective means of distributing elite rhizobial strains to broad-acre crops and pastures. However, necessary drying steps after coating seed expose rhizobia to desiccation stress reducing survival and limiting potential nitrogen fixation by legumes. Rhizobial tolerance to desiccation varies with strain and with growth conditions prior to drying. Cells grown in peat generally survive desiccation better than cells grown in liquid broth. We aimed to identify peat-induced proteomic changes in rhizobia that may be linked to desiccation tolerance. Proteins expressed differentially after growth in peat extract when compared with a minimal defined medium were measured in four rhizobial strains. Proteins showing the greatest increase in abundance were those involved in amino acid and carbohydrate transport and metabolism. Proteins involved in posttranslational modification and cell defence mechanisms were also upregulated. Many of the proteins identified in this study have been previously linked to stress responses. In addition, analysis using nucleic acid stains SYTO9 and propidium iodide indicated that membranes had been compromised after growth in peat extract. We targeted the membrane repair protein PspA (ΔRL3579) which was upregulated in Rhizobium leguminosarum bv. viceae 3841 after growth in peat extract to validate whether the inability to repair membrane damage after growth in peat extract reduced desiccation tolerance. The ΔRL3579 mutant grown in peat extract had significantly lower survival under desiccation stress, whereas no difference in survival between wild-type and mutant strains was observed after growth in tryptone yeast (TY) or minimal medium (JMM) media. Staining mutant and wild-type strains with SYTO9 and propidium iodide indicated that membranes of the mutant were compromised after growth in peat extract and to a lesser extent in TY. This study shows that growth in peat extract causes damage to cell membranes and exposes rhizobia to sub-lethal stress resulting in differential expression of several stress-induced proteins. The induction of these proteins may prime and protect the cells when subjected to subsequent stress such as desiccation. Identifying the key proteins involved in desiccation tolerance and properties of peat that stimulate this response will be important to inform development of new inoculant technology that maximises survival of rhizobia during delivery to legume crops and pastures.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Acebrón SP, Martín I, del Castillo U, Moro F, Muga A (2009) DnaK-mediated association of ClpB to protein aggregates. A bichaperone network at the aggregate surface. FEBS Lett 583(18):2991–2996

    Article  PubMed  CAS  Google Scholar 

  • Albareda M, Rodríguez-Navarro DN, Camacho M, Temprano FJ (2008) Alternatives to peat as a carrier for rhizobia inoculants: solid and liquid formulations. Soil Biol Biochem 40(11):2771–2779

    Article  CAS  Google Scholar 

  • Alexandre A, Laranjo M, Oliveira S (2013) Global transcriptional response to heat shock of the legume symbiont Mesorhizobium loti MAFF303099 comprises extensive gene downregulation. DNA Res 21:195–206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Atieno M, Herrmann L, Okalebo R, Lesueur D (2012) Efficiency of different formulations of Bradyrhizobium japonicum and effect of co-inoculation of Bacillus subtilis with two different strains of Bradyrhizobium japonicum. World J Microbiol Biotechnol 28(7):2541–2550

    Article  PubMed  CAS  Google Scholar 

  • Balestrino D, Ghigo JM, Charbonnel N, Haagensen JA, Forestier C (2008) The characterization of functions involved in the establishment and maturation of Klebsiella pneumoniae in vitro biofilm reveals dual roles for surface exopolysaccharides. Environ Microbiol 10(3):685–701

    Article  PubMed  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE, Prabhu S, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378(1–2):1–33

    Article  CAS  Google Scholar 

  • Batista JSD, Torres AR, Hungria M (2010) Towards a two-dimensional proteomic reference map of Bradyrhizobium japonicum CPAC 15: spotlighting “hypothetical proteins”. Proteomics 10(17):3176–3189

    Article  PubMed  CAS  Google Scholar 

  • Beringer JE (1974) R Factor transfer in Rhizobium leguminosarum. Microbiol 84(1):188–198

    Article  CAS  Google Scholar 

  • Biter AB, Lee S, Sung N, Tsai FT (2012) Structural basis for intersubunit signaling in a protein disaggregating machine. Proc Natl Acad Sci U S A 109(31):12515–12520

    Article  PubMed  PubMed Central  Google Scholar 

  • Brígido C, Robledo M, Menéndez E, Mateos PF, Oliveira S (2012) A ClpB chaperone knockout mutant of Mesorhizobium ciceri shows a delay in the root nodulation of chickpea plants. Mol Plant-Microbe Interact 25(12):1594–1604

    Article  PubMed  CAS  Google Scholar 

  • Brockwell J, Herridge DF, Roughley RJ, Thompson JA, Gault RR (1975) Studies on seed pelleting as an aid to legume seed inoculation. 4. Examination of preinoculated seed. Aust J Exp Agric Anim Husb 15:780–787

    Article  Google Scholar 

  • Browning DF, Busby SJW (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2(1):57–65

    Article  PubMed  CAS  Google Scholar 

  • Casteriano A, Wilkes MA, Deaker R (2013) Physiological changes in rhizobia after growth in peat extract may be related to improved desiccation tolerance. Appl Environ Microbiol 79(13):3998–4007

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cytryn EJ, Sangurdekar DP, Streeter JG, Franck WL, Chang WS, Stacey G, Emerich DW, Joshi T, Xu D, Sadowsky MJ (2007) Transcriptional and physiological responses of Bradyrhizobium japonicum to desiccation-induced stress. J Bacteriol 189(19):6751–6762

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • da Silva Batista JS, Hungria M (2012) Proteomics reveals differential expression of proteins related to a variety of metabolic pathways by genistein-induced Bradyrhizobium japonicum strains. J Proteome 75(4):1211–1219

    Article  CAS  Google Scholar 

  • Dart P, Roughley R, Chandler MR (1969) Peat culture of Rhizobium trifolii: an examination by electron microscopy. J Appl Microbiol 32(3):352–357

    Google Scholar 

  • Davey HM, Hexley P (2011) Red but not dead? Membranes of stressed Saccharomyces cerevisiae are permeable to propidium iodide. 13:163–171. https://doi.org/10.1111/j.1462-2920.2010.02317.x

  • Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology: a review. Soil Biol Biochem 36(8):1275–1288

    Article  CAS  Google Scholar 

  • Deaker R, Hartley E, Gemell G (2012) Conditions affecting shelf-life of inoculated legume seed. Agric J 2(1):38–51

    Google Scholar 

  • DeLisa MP, Lee P, Palmer T, Georgiou G (2003) Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J Bacteriol 186(2):366–373

    Article  CAS  Google Scholar 

  • Deaker R, Roughley RJ, Kennedy IR (2007) Desiccation tolerance of rhizobia when protected by synthetic polymers. Soil Biol Biochem 39:573–580. https://doi.org/10.1016/j.soilbio.2006.09.005

    Article  CAS  Google Scholar 

  • El-Sharoud WM (2004) Ribosome inactivation for preservation: concepts and reservations. Sci Prog 87(Pt 3):137–152

    Article  PubMed  CAS  Google Scholar 

  • Encarnación S, Guzmán Y, Dunn MF, Hernández M, del Vargas M, Mora J (2003) Proteome analysis of aerobic and fermentative metabolism in Rhizobium etli CE3. Proteomics 3(6):1077–1085

    Article  PubMed  CAS  Google Scholar 

  • Feng L, Roughley RJ, Copeland L (2002) Morphological changes of Rhizobia in peat cultures. Appl Environ Microbiol 68(3):1064–1070

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Figurski D, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependent. Proc Natl Acad Sci U S A 76:1648–1652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • França M, Panek A, Eleutherio E (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A Mol Integr Physiol 146(4):621–631

    Article  PubMed  CAS  Google Scholar 

  • Francez-Charlot A, Kaczmarczyk A, Fischer HM, Vorholt JA (2015) The general stress response in Alphaproteobacteria. Trends Microbiol 23(3):164–171

    Article  PubMed  CAS  Google Scholar 

  • Fu C, Donovan WP, Shikapwashya-Hasser O, Ye X, Cole RH (2014) Hot fusion: an efficient method to clone multiple DNA fragments as well as inverted repeats without ligase. PLoS One 9(12):e115318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gemell LGA, Hartley EJA, Herridge DFB (2005) Point-of-sale evaluation of preinoculated and custom-inoculated pasture legume seed. Aust J Exp Agric 45:161–169

    Article  Google Scholar 

  • Gez S, Crossett B, Christopherson RI (2007) Differentially expressed cytosolic proteins in human leukemia and lymphoma cell lines correlate with lineages and functions. Biochim Biophys Acta, Proteins Proteomics 1774(9):1173–1183

    Article  CAS  Google Scholar 

  • Gilbert KB, Vanderlinde EM, Yost CK (2007) Mutagenesis of the carboxy terminal protease CtpA decreases desiccation tolerance in Rhizobium leguminosarum. FEMS Microbiol Lett 272(1):65–74

    Article  PubMed  CAS  Google Scholar 

  • Glenn R, Poole PS, Hudman JF (1980) SHORT COMMUNICATION Succinate Uptake by Free-living and Bacteroid Forms of Rhizobium leguminosarum. J Gen Microbiol 119:267–271

    CAS  Google Scholar 

  • Gourion B, Sulser S, Frunzke J, Francez-Charlot A, Stiefel P, Pessi G, Vorholt JA, Fischer H-M (2009) The PhyR-σEcfG signalling cascade is involved in stress response and symbiotic efficiency in Bradyrhizobium japonicum. Mol Microbiol 73(2):291–305

    Article  PubMed  CAS  Google Scholar 

  • Gutsche I, Essen L-O, Baumeister W (1999) Group II chaperonins: new TRiC (k) s and turns of a protein folding machine. J Mol Biol 293(2):295–312

    Article  PubMed  CAS  Google Scholar 

  • Hartley EJ, Gemell LG, Deaker R (2012) Some factors that contribute to poor survival of rhizobia on preinoculated legume seed. Crop Pasture Sci 63(9):858–865

    Article  Google Scholar 

  • Heipieper H, Keweloh H, Rehm H (1991) Influence of Phenols on Growth and Membrane Permeability of Free and Immobilized Escherichia coli. Appl Environ Microbiol 57:1213–1217

    PubMed  PubMed Central  CAS  Google Scholar 

  • Henrich S, Cordwell SJ, Crossett B, Baker MS, Christopherson RI (2007) The nuclear proteome and DNA-binding fraction of human Raji lymphoma cells. Biochim Biophys Acta 1774(4):413–432

    Article  PubMed  CAS  Google Scholar 

  • Herrmann L, Lesueur D (2013) Challenges of formulation and quality of biofertilizers for successful inoculation. Appl Microbiol Biotechnol 97(20):8859–8873

    Article  PubMed  CAS  Google Scholar 

  • Hiller K, Grote A, Maneck M, Münch R, Jahn D (2006) JVirGel 2.0: computational prediction of proteomes separated via two-dimensional gel electrophoresis under consideration of membrane and secreted proteins. Bioinformatics 22(19):2441–2443

    Article  PubMed  CAS  Google Scholar 

  • Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77(1):61–68

    Article  PubMed  CAS  Google Scholar 

  • Humann JL, Kahn ML (2015) Genes involved in desiccation resistance of rhizobia and other bacteria. In: de Bruijn FJ (ed) Biological nitrogen fixation. Volume 1. John Wiley & Sons, Inc, New Jersey, pp 397–404

    Chapter  Google Scholar 

  • Johnston A, Beringer J (1975) Identification of the Rhizobium Strains in Pea Root Nodules Using Genetic Markers. J Gen Microbiol 87:343–350

    Article  PubMed  CAS  Google Scholar 

  • Jones KM, Walker GC (2008) Responses of the model legume Medicago truncatula to the rhizobial exopolysaccharide succinoglycan. Plant Signal Behav 3(10):888–890

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9(6):189–197

    Article  PubMed  Google Scholar 

  • Kedzierska S, Matuszewska E (2001) The effect of co-overproduction of DnaK/DnaJ/GrpE and ClpB proteins on the removal of heat-aggregated proteins from Escherichia coli ΔclpB mutant cells—new insight into the role of Hsp70 in a functional cooperation with Hsp100. FEMS Microbiol Lett 204(2):355–360

    PubMed  CAS  Google Scholar 

  • Kim HS, Willett JW, Jain-Gupta N, Fiebig A, Crosson S (2014) The Brucella abortus virulence regulator, LovhK, is a sensor kinase in the general stress response signalling pathway. Mol Microbiol 94(4):913–925

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kleerebezem M, Crielaard W, Tommassen J (1996) Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the proton-motive force under stress conditions. EMBO J 15(1):162–171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kobayashi H, Yamamoto M, Aono R (1998) Appearance of a stress-response protein, phage-shock protein A, in Escherichia coli exposed to hydrophobic organic solvents. Microbiol 144(2):353–359

    Article  CAS  Google Scholar 

  • Kobayashi R, Suzuki T, Yoshida M (2007) Escherichia coli phage-shock protein a (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol Microbiol 66(1):100–109

    Article  PubMed  CAS  Google Scholar 

  • Lesueur D, Deaker R, Herrmann L, Bräu L, Jansa J (2016) The production and potential of biofertilizers to improve crop yields. In: Arora NK, Mehnaz S, Balestrini R (eds) Bioformulations: for sustainable agriculture. Springer, New Delhi, pp 71–92

    Google Scholar 

  • Li J, Xiao W-L, Ma M-C, Guan D-W, Jiang X, Cao F-M, Shen D-L, Chen H-J, Li L (2011) Proteomic study on two Bradyrhizobium japonicum strains with different competitivenesses for nodulation. Agric Sci China 10(7):1072–1079

    Article  CAS  Google Scholar 

  • Model P, Jovanovic G, Dworkin J (1997) The Escherichia coli phage-shock-protein (psp) operon. Mol Microbiol 24(2):255–261

    Article  PubMed  CAS  Google Scholar 

  • Neudorf KD, Vanderlinde EM, Tambalo DD, Yost CK (2015) A previously uncharacterized tetratricopeptide-repeat-containing protein is involved in cell envelope function in Rhizobium leguminosarum. Microbiology 161(1):148–157

    Article  PubMed  CAS  Google Scholar 

  • O’Brien KM, Dirmeier R, Engle M, Poyton RO (2004) Mitochondrial protein oxidation in yeast mutants lacking manganese-(MnSOD) or copper-and zinc-containing superoxide dismutase (CuZnSOD): evidence that MnSOD AND CuZnSOD have both unique and overlapping functions in protecting mitochondrial proteins from oxidative damage. J Biol Chem 279(50):51817–51827

    Article  PubMed  CAS  Google Scholar 

  • O’Hara GW, Goss TJ, Dilworth MJ, Glenn AR (1989) Maintenance of intracellular pH and acid tolerance in Rhizobium meliloti. Appl Environ Microbiol 55(8):1870–1876

    PubMed  PubMed Central  Google Scholar 

  • Ophir T, Gutnick DL (1994) A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol 60(2):740–745

    PubMed  PubMed Central  CAS  Google Scholar 

  • Paço A, Brígido C, Alexandre A, Mateos PF, Oliveira S (2016) The symbiotic performance of chickpea rhizobia can be improved by additional copies of the clpB chaperone gene. PLoS One 11(2):e0148221

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Hérouart D, Frendo P, Puppo A (2006) Reactive oxygen and nitrogen species and glutathione: key players in the legume–Rhizobium symbiosis. J Exp Bot 57(8):1769–1776

    Article  PubMed  CAS  Google Scholar 

  • Poole PS, Schofiel NA, Reid CJ, Drew EM, Walshaw DL (1994) Identification of chromosomal genes located downstream of dctD that affect the requirement for calcium and the lipopolysaccharide layer of Rhizobium leguminosarum. Microbiol 140(10):2797–2809

    Article  CAS  Google Scholar 

  • Prell J, White J, Bourdes A, Bunnewell S, Bongaerts R, Poole P (2009) Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc Natl Acad Sci U S A 106(30):12477–12482

    Article  PubMed  PubMed Central  Google Scholar 

  • Quandt J, Hynes MF (1993) Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127(1):15–21

    Article  PubMed  CAS  Google Scholar 

  • Queitsch C, Hong S-W, Vierling E, Lindquist S (2000) Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12(4):479–492

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Raju RM, Jedrychowski MP, Wei J-R, Pinkham JT, Park AS, O’Brien K, Rehren G, Schnappinger D, Gygi SP, Rubin EJ (2014) Post-translational regulation via Clp protease is critical for survival of Mycobacterium tuberculosis. PLoS Pathog 10(3):e1003994

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Russo DM, Williams A, Edwards A, Posadas DM, Finnie C, Dankert M, Downie JA, Zorreguieta A (2006) Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum. J Bacteriol 188(12):4474–4486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Press, New York

    Google Scholar 

  • Sarma AD, Emerich DW (2005) Global protein expression pattern of Bradyrhizobium japonicum bacteroids: a prelude to functional proteomics. Proteomics 5(16):4170–4184

    Article  PubMed  CAS  Google Scholar 

  • Shirkey B, Kovarcik DP, Wright DJ, Wilmoth G, Prickett TF, Helm RF, Gregory EM, Potts M (2000) Active Fe-containing superoxide dismutase and abundant sodF mRNA in Nostoc commune (Cyanobacteria) after years of desiccation. J Bacteriol 182(1):189–197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simonin H, Beney L, Gervais P (2007) Sequence of occurring damages in yeast plasma membrane during dehydration and rehydration : Mechanisms of cell death. i:1600–1610. https://doi.org/10.1016/j.bbamem.2007.03.017

  • Siqueira AF, Ormeño-Orrillo E, Souza RC, Rodrigues EP, Almeida LGP, Barcellos FG, Batista JSS, Nakatani AS, Martínez-Romero E, Vasconcelos ATR, Hungria M (2014) Comparative genomics of Bradyrhizobium japonicum CPAC 15 and Bradyrhizobium diazoefficiens CPAC 7: elite model strains for understanding symbiotic performance with soybean. BMC Genomics 15(1):420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Standar K, Mehner D, Osadnik H, Berthelmann F, Hause G, Lünsdorf H, Brüser T (2008) PspA can form large scaffolds in Escherichia coli. FEBS Lett 582(25–26):3585–3589

    Article  PubMed  CAS  Google Scholar 

  • Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crops Res 65(2–3):249–258

    Article  Google Scholar 

  • Vanderlinde EM, Yost CK (2012) Genetic analysis reveals links between lipid a structure and expression of the outer membrane protein gene, ropB, in Rhizobium leguminosarum. FEMS Microbiol Lett 335:130–139. https://doi.org/10.1111/j.1574-6968.2012.02645.x

    Article  PubMed  CAS  Google Scholar 

  • Vanderlinde EM, Muszyński A, Harrison JJ, Koval SF, Foreman DL, Ceri H, Kannenberg EL, Carlson RW, Yost CK (2009) Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired indesiccation tolerance, biofilm formation and motility. Microbiology 155:3055–3069. https://doi.org/10.1099/mic.0.025031-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vanderlinde EM, Harrison JJ, Muszyński A, Carlson RW, Turner RJ, Yost CK (2010) Identification of a novel ABC transporter required for desiccation tolerance, and biofilm formation in Rhizobium leguminosarum bv. viciae 3841. FEMS Microbiol Ecol 71(3):327–340

    Article  PubMed  CAS  Google Scholar 

  • Vanderlinde EM, Magnus SA, Tambalo DD, Koval SF, Yost CK (2011) Mutation of a broadly conserved operon (RL3499-RL3502) from Rhizobium leguminosarum biovar viciae causes defects in cell morphology and envelope integrity. J Bacteriol 193:2684–2694. https://doi.org/10.1128/JB.01456-10

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vriezen JAC, de Bruijn FJ, Nüsslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl Environ Microbiol 73:3451–3459. https://doi.org/10.1128/AEM.02991-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vizcaino JA, Cote RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J, O’Kelly G, Schoenegger A, Ovelleiro D, Perez-Riverol Y, Reisinger F, Rios D, Wang R, Hermjakob H (2013) The Proteomics Identifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 41(D1):D1063–D1069. https://doi.org/10.1093/nar/gks1262

    Article  PubMed  CAS  Google Scholar 

  • Weiner L, Model P (1994) Role of an Escherichia coli stress-response operon in stationary-phase survival. Proc Natl Acad Sci U S A 91(6):2191–2195

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamaguchi S, Gueguen E, Horstman NK, Darwin AJ (2010) Membrane association of PspA depends on activation of the phage-shock-protein response in Yersinia enterocolitica. Mol Microbiol 78(2):429–443

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Young JPW, Crossman LC, Johnston AW, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson AR, Todd JD, Poole PS (2006) The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol 7(4):R34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the facilities, as well as the scientific and technical assistance from the Mass Spectrometry Core Facility at the University of Sydney.

Funding

This study was funded by the Australia Awards and Grains Research and Development Corporation (GRS135 and US00065) through the University of Sydney.

Author information

Authors and Affiliations

  1. School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia

    Mary Atieno, Neil Wilson & Rosalind Deaker

  2. Koala Health Hub, University of Sydney, Sydney, NSW, Australia

    Andrea Casteriano

  3. Mass Spectrometry Core Facility, University of Sydney, Sydney, NSW, Australia

    Ben Crossett

  4. Eco&Sols, University Montpellier, CIRAD, Montpellier, France

    Didier Lesueur

  5. CIRAD, UMR Eco&Sols, CIAT-Asia, Hanoi, Vietnam

    Didier Lesueur

  6. Deakin University, Melbourne, Australia

    Didier Lesueur

Authors
  1. Mary Atieno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neil Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andrea Casteriano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ben Crossett
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Didier Lesueur
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rosalind Deaker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mary Atieno.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Mary Atieno and Neil Wilson are joint first authors.

Electronic supplementary material

ESM 1

(PDF 3825 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Atieno, M., Wilson, N., Casteriano, A. et al. Aqueous peat extract exposes rhizobia to sub-lethal stress which may prime cells for improved desiccation tolerance. Appl Microbiol Biotechnol 102, 7521–7539 (2018). https://doi.org/10.1007/s00253-018-9086-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-018-9086-2

Keywords

Search

Navigation