Advertisement

Applied Microbiology and Biotechnology

, Volume 102, Issue 17, pp 7521–7539 | Cite as

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

  • Mary Atieno
  • Neil Wilson
  • Andrea Casteriano
  • Ben Crossett
  • Didier Lesueur
  • Rosalind Deaker
Genomics, transcriptomics, proteomics

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.

Keywords

Rhizobia Inoculant technology Desiccation tolerance Peat 

Notes

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.

Compliance with ethical standards

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.

Supplementary material

253_2018_9086_MOESM1_ESM.pdf (3.7 mb)
ESM 1 (PDF 3825 kb)

References

  1. 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):2991–2996CrossRefPubMedGoogle Scholar
  2. 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):2771–2779CrossRefGoogle Scholar
  3. 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 21:195–206CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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):2541–2550CrossRefPubMedGoogle Scholar
  5. 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):685–701CrossRefPubMedGoogle Scholar
  6. 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):1–33CrossRefGoogle Scholar
  7. 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):3176–3189CrossRefPubMedGoogle Scholar
  8. Beringer JE (1974) R Factor transfer in Rhizobium leguminosarum. Microbiol 84(1):188–198CrossRefGoogle Scholar
  9. 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):12515–12520CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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):1594–1604CrossRefPubMedGoogle Scholar
  11. 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 15:780–787CrossRefGoogle Scholar
  12. Browning DF, Busby SJW (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2(1):57–65CrossRefPubMedGoogle Scholar
  13. 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):3998–4007CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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):6751–6762CrossRefPubMedPubMedCentralGoogle Scholar
  15. 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):1211–1219CrossRefGoogle Scholar
  16. Dart P, Roughley R, Chandler MR (1969) Peat culture of Rhizobium trifolii: an examination by electron microscopy. J Appl Microbiol 32(3):352–357Google Scholar
  17. 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
  18. Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology: a review. Soil Biol Biochem 36(8):1275–1288CrossRefGoogle Scholar
  19. Deaker R, Hartley E, Gemell G (2012) Conditions affecting shelf-life of inoculated legume seed. Agric J 2(1):38–51Google Scholar
  20. 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):366–373CrossRefGoogle Scholar
  21. 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 CrossRefGoogle Scholar
  22. El-Sharoud WM (2004) Ribosome inactivation for preservation: concepts and reservations. Sci Prog 87(Pt 3):137–152CrossRefPubMedGoogle Scholar
  23. 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):1077–1085CrossRefPubMedGoogle Scholar
  24. Feng L, Roughley RJ, Copeland L (2002) Morphological changes of Rhizobia in peat cultures. Appl Environ Microbiol 68(3):1064–1070CrossRefPubMedPubMedCentralGoogle Scholar
  25. Figurski D, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependent. Proc Natl Acad Sci U S A 76:1648–1652CrossRefPubMedPubMedCentralGoogle Scholar
  26. França M, Panek A, Eleutherio E (2007) Oxidative stress and its effects during dehydration. Comp Biochem Physiol A Mol Integr Physiol 146(4):621–631CrossRefPubMedGoogle Scholar
  27. Francez-Charlot A, Kaczmarczyk A, Fischer HM, Vorholt JA (2015) The general stress response in Alphaproteobacteria. Trends Microbiol 23(3):164–171CrossRefPubMedGoogle Scholar
  28. 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):e115318CrossRefPubMedPubMedCentralGoogle Scholar
  29. Gemell LGA, Hartley EJA, Herridge DFB (2005) Point-of-sale evaluation of preinoculated and custom-inoculated pasture legume seed. Aust J Exp Agric 45:161–169CrossRefGoogle Scholar
  30. 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):1173–1183CrossRefGoogle Scholar
  31. 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):65–74CrossRefPubMedGoogle Scholar
  32. Glenn R, Poole PS, Hudman JF (1980) SHORT COMMUNICATION Succinate Uptake by Free-living and Bacteroid Forms of Rhizobium leguminosarum. J Gen Microbiol 119:267–271Google Scholar
  33. 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):291–305CrossRefPubMedGoogle Scholar
  34. 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):295–312CrossRefPubMedGoogle Scholar
  35. 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):858–865CrossRefGoogle Scholar
  36. Heipieper H, Keweloh H, Rehm H (1991) Influence of Phenols on Growth and Membrane Permeability of Free and Immobilized Escherichia coli. Appl Environ Microbiol 57:1213–1217PubMedPubMedCentralGoogle Scholar
  37. 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):413–432CrossRefPubMedGoogle Scholar
  38. Herrmann L, Lesueur D (2013) Challenges of formulation and quality of biofertilizers for successful inoculation. Appl Microbiol Biotechnol 97(20):8859–8873CrossRefPubMedGoogle Scholar
  39. 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):2441–2443CrossRefPubMedGoogle Scholar
  40. 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):61–68CrossRefPubMedGoogle Scholar
  41. 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 397–404CrossRefGoogle Scholar
  42. Johnston A, Beringer J (1975) Identification of the Rhizobium Strains in Pea Root Nodules Using Genetic Markers. J Gen Microbiol 87:343–350CrossRefPubMedGoogle Scholar
  43. Jones KM, Walker GC (2008) Responses of the model legume Medicago truncatula to the rhizobial exopolysaccharide succinoglycan. Plant Signal Behav 3(10):888–890CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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):189–197CrossRefPubMedGoogle Scholar
  45. 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):355–360PubMedGoogle Scholar
  46. 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):913–925CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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):162–171PubMedPubMedCentralGoogle Scholar
  48. 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):353–359CrossRefGoogle Scholar
  49. 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):100–109CrossRefPubMedGoogle Scholar
  50. 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 71–92Google Scholar
  51. 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):1072–1079CrossRefGoogle Scholar
  52. Model P, Jovanovic G, Dworkin J (1997) The Escherichia coli phage-shock-protein (psp) operon. Mol Microbiol 24(2):255–261CrossRefPubMedGoogle Scholar
  53. 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):148–157CrossRefPubMedGoogle Scholar
  54. 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):51817–51827CrossRefPubMedGoogle Scholar
  55. 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):1870–1876PubMedPubMedCentralGoogle Scholar
  56. Ophir T, Gutnick DL (1994) A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol 60(2):740–745PubMedPubMedCentralGoogle Scholar
  57. 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):e0148221CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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):1769–1776CrossRefPubMedGoogle Scholar
  59. 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):2797–2809CrossRefGoogle Scholar
  60. 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):12477–12482CrossRefPubMedPubMedCentralGoogle Scholar
  61. Quandt J, Hynes MF (1993) Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127(1):15–21CrossRefPubMedGoogle Scholar
  62. 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):479–492CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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):e1003994CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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):4474–4486CrossRefPubMedPubMedCentralGoogle Scholar
  65. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Press, New YorkGoogle Scholar
  66. Sarma AD, Emerich DW (2005) Global protein expression pattern of Bradyrhizobium japonicum bacteroids: a prelude to functional proteomics. Proteomics 5(16):4170–4184CrossRefPubMedGoogle Scholar
  67. 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):189–197CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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
  69. 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):420CrossRefPubMedPubMedCentralGoogle Scholar
  70. 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):3585–3589CrossRefPubMedGoogle Scholar
  71. Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crops Res 65(2–3):249–258CrossRefGoogle Scholar
  72. 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 CrossRefPubMedGoogle Scholar
  73. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 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):327–340CrossRefPubMedGoogle Scholar
  75. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 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 CrossRefPubMedGoogle Scholar
  78. 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):2191–2195CrossRefPubMedPubMedCentralGoogle Scholar
  79. 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):429–443CrossRefPubMedPubMedCentralGoogle Scholar
  80. 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):R34CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia
  2. 2.Koala Health HubUniversity of SydneySydneyAustralia
  3. 3.Mass Spectrometry Core FacilityUniversity of SydneySydneyAustralia
  4. 4.Eco&Sols, University Montpellier, CIRADMontpellierFrance
  5. 5.CIRAD, UMR Eco&Sols, CIAT-AsiaHanoiVietnam
  6. 6.Deakin UniversityMelbourneAustralia

Personalised recommendations