Log in

Effect of Oxygen on the Growth and Biofilm Formation of Xylella fastidiosa in Liquid Media

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Xylella fastidiosa is a xylem-limited bacterial pathogen, and is the causative agent of Pierce’s disease of grapevines and scorch diseases of many other plant species. The disease symptoms are putatively due to blocking of the transpiration stream by bacterial-induced biofilm formation and/or by the formation of plant-generated tylosis. Xylella fastidiosa has been classified as an obligate aerobe, which appears unusual given that dissolved O2 levels in the xylem during the growing season are often hypoxic (20–60 μmol L−1). We examined the growth and biofilm formation of three strains of X. fastidiosa under variable O2 conditions (21, 2.1, 0.21 and 0 % O2), in comparison to that of Pseudomonas syringae (obligate aerobe) and Erwinia carotovora (facultative anaerobe) under similar conditions. The growth of X. fastidiosa more closely resembled that of the facultative anaerobe, and not the obligate aerobe. Xanthomonas campestris, the closest genetic relative of X. fastidiosa, exhibited no growth in an N2 environment, whereas X. fastidiosa was capable of growing in an N2 environment in PW+, CHARDS, and XDM2-PR media. The magnitude of growth and biofilm formation in the N2 (0 % O2) treatment was dependent on the specific medium. Additional studies involving the metabolism of X. fastidiosa in response to low O2 are warranted. Whether X. fastidiosa is classified as an obligate aerobe or a facultative anaerobe should be confirmed by gene activation and/or the quantification of the metabolic profiles under hypoxic conditions.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  1. Andersen PC, Brodbeck BV (1989) Diurnal and temporal changes in the chemical profile of xylem exudate from Vitis rotundifolia. Physiol Plant 75:63–70

    Article  CAS  Google Scholar 

  2. Andersen PC, Brodbeck BV (1991) Influence of fertilization on xylem fluid chemistry of Vitis rotundifolia Noble and Vitis hybrid Suwannee. Am J Enol Vitic 42:245–251

    CAS  Google Scholar 

  3. Andersen PC, Brodbeck BV, Mizell RF III (1992) Feeding by the leafhopper, Homalodisca coagulata, in relation to xylem fluid chemistry and tension. J Insect Physiol 38:611–622

    Article  CAS  Google Scholar 

  4. Andersen PC, Brodbeck BV, Oden S, Shriner AD, Leite B (2007) Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa. FEMS Microbiol Lett 274:210–217

    Article  PubMed  CAS  Google Scholar 

  5. Andersen PC, French WJ (1987) Biophysical characteristics of peach trees infected with phony peach disease. Physiol Mol Plant Pathol 31:25–40

    Article  Google Scholar 

  6. Barbosa RL, Benedetti CE (2007) BigR, a transcriptional repressor from plant-associated bacteria, regulates an operon implicated in biofilm growth. J Bacteriol 189:6185–6194

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  7. Caserta R, Takita MA, Targon ML, Rosselli-Murai LK, de Souza AP, Peroni L, Stach-Machado DR, Andrade A, Labate CA, Kitajima EW, Machado MA, de Souza AA (2010) Expression of Xylella fastidiosa fimbrial and afimbrial proteins during biofilm formation. Appl Eviron Microbiol 76:4250–4259

    Article  CAS  Google Scholar 

  8. Chatterjee S, Almeida RPP, Lindow S (2008) Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Ann Rev Phytopathol 46:243–271

    Article  CAS  Google Scholar 

  9. Chen PC, **e G, Han S, Chertkov O, Sims D, Civerolo EL (2010) Whole genome sequences of two Xylella fastidiosa strains (M12 and M23) causing almond leaf scorch disease in California. J Bacteriol 192:4534

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Costerton JW, Lewandowski Z, Calswell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Ann Rev Microbiol 49:711–745

    Article  CAS  Google Scholar 

  11. Davis MJ, French WJ, Schaad NW (1981) Axenic culture of the bacteria associated with phony disease of peach and plum leaf scald. Curr Microbiol 6:309–314

    Article  Google Scholar 

  12. Dongen JTV, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 1331:1529–1543

    Article  Google Scholar 

  13. Eklund L (2000) Internal oxygen levels decrease during the growing season and with increasing stem height. Trees 14:177–180

    Article  Google Scholar 

  14. Esau K (1948) Anatomic effects of the viruses of Pierce’s disease and phony peach. Hilgardia 18:423–482

    Article  Google Scholar 

  15. Espinosa-Urgel M, Salido A, Ramos J-L (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182:2363–2369

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  16. Fritschi FB, Lin H, Walker MA (2008) Scanning electron microscopy reveals different response pattern of four Vitis genotypes to Xylella fastidiosa infection. Plant Dis 92:276–286

    Article  Google Scholar 

  17. Gambetta GA, Fei J, Rost TL, Matthews MA (2007) Leaf scorch symptoms are not correlated with bacterial populations during Pierce’s disease. J Exp Bot 58:4037–4046

    Article  PubMed  CAS  Google Scholar 

  18. Gansert D, Burgdorf M, Losch R (2001) A novel approach to the in situ measurement of oxygen concentrations in the sapwood of woody plants. Plant Cell Environ 24:1055–1064

    Article  CAS  Google Scholar 

  19. Gansert D (2003) Xylem sap flow as a major pathway for oxygen supply to the sapwood of birch (Betula pubescens Ehr.). Plant Cell Environ 26:803–1814

    Article  Google Scholar 

  20. Goodwin PH, DeVay JE, Meredith CP (1988) Roles of water stress and phytotoxins in the development of Pierce’s disease of the grapevine. Physiol Mol Plant Pathol 32:1–15

    Article  CAS  Google Scholar 

  21. Guimareaes BG, Barbosa RL, Soprano AS, Campos BM, de Souza TA, Tonoli CCC, Leme AFP, Murakami T, Benedetti CE (2011) Plant pathogenic bacteria utilize biofilm growth-associated repressor (BigR), a novel winged-helix redox switch to control hydrogen sulfide detoxification under hypoxia. J Biol Chem 286:26148–26157

    Article  Google Scholar 

  22. Hierro AMD, Kronberger W, Heitz P, Offenthaler I, Richter H (2002) A new method to determine the oxygen concentration inside the sapwood of trees. J Exp Bot 53:559–563

    Article  PubMed  Google Scholar 

  23. Killiny N, Hernando Martinez R, Korsi Dumenyo C, Cooksey DA, Almeida RPP (2013) The exopolysaccharide of Xylella fastidiosa is essential for biofilm formation, plant virulence and vector transmission. Mol Plant Microb Interact 26:1044–1053

    Article  CAS  Google Scholar 

  24. Kimmerer TW, Stringer MA (1988) Alcohol dehydrogenase and ethanol in the stems of trees: evidence for the anaerobic metabolism in the vascular cambium. Plant Physiol 87:693–697

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  25. Krivanek AF, Stevenson JF, Walker MA (2005) Development and comparison of symptom indices for quantifying grapevine resistance to Pierce’s disease. Phytopathology 95:36–43

    Article  PubMed  CAS  Google Scholar 

  26. Leite B, Andersen PC, Ishida ML (2004) Colony aggregation and biofilm formation in xylem chemistry-based media for Xylella fastidiosa. FEMS Microbiol Lett 230:283–290

    Article  PubMed  CAS  Google Scholar 

  27. Lemos EG, Alves LM, Campanharo JC (2003) Genomics-based design of defined growth media for the plant pathogen Xylella fastidiosa. FEMS Microbiol Lett 219:39–45

    Article  PubMed  CAS  Google Scholar 

  28. Lorite GS, Rodrigues CM, de Souza AA, Kranz C, Mizaikoff Cotta MA (2011) The role conditioning film formation and surface chemical changes on Xylella fastidiosa adhesion and biofilm evolution. J Colloid Interface Sci 359:289–295

    Article  PubMed  CAS  Google Scholar 

  29. MacDonald RC, Kimmerer TW (1991) Ethanol in the stems of trees. Plant Physiol 82:582–588

    Article  CAS  Google Scholar 

  30. MacDonald RC, Kimmerer TW (1993) Metabolism of transpired ethanol by eastern cottonwood (Populus deltoides Bartr.). Plant Physiol 102:173–179

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Mancuso S, Boselli M (2002) Characterisation of the oxygen fluxes in the division, elongation, and mature zones of Vitis roots: influence of oxygen availability. Planta 214:767–774

    Article  PubMed  CAS  Google Scholar 

  32. Mancuso S, Marras AM (2003) Different pathways of the oxygen supply in the sapwood of young Olea europaea trees. Planta 216:1028–1033

    PubMed  CAS  Google Scholar 

  33. Marques LLR, Ceri H, Manfio GP, Reid DM, Olson ME (2002) Characterization of biofilm formation by Xylella fastidiosa in vitro. Plant Dis 86:633–638

    Article  Google Scholar 

  34. Nunney L, Vickerman DB, Bromlet RE, Russell SA, Hartman JR, Morano LD, Stouthamer R (2013) Recent evolutionary radiation and host plant specialization in the Xylella fastidiosa subspecies native to the United States. Appl Environ Microbiol 79:2189–2200

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  35. Pooler MR, Hartung JS (1995) Genetic relationships among strains of Xylella fastidiosa from RAPD-PCR data. Curr Microbiol 31:134–137

    Article  PubMed  CAS  Google Scholar 

  36. Purcell AH, Hopkins DL (1996) Fastidious xylem-limited bacterial plant pathogens. Ann Rev Phytopathol 34:131–151

    Article  CAS  Google Scholar 

  37. Schaad NW, Postnikova E, Lacy G, Fatmi M’B, Chang C-J (2004) Xylella fastidiosa subspecies: X. fastidiosa subsp. piercei, subsp. nov., X. fastidiosa subsp. multiplex subsp. nov., and X. fastidiosa subsp. pauca subsp. nov. Syst Appl Microbiol 27:290–300

    Article  PubMed  CAS  Google Scholar 

  38. Shi X, Bi J, Morse JG, Toscano NC, Cooksey DA (2013) Effect of xylem fluid from susceptible and resistant grapevines on developmental biology of Xylella fastidiosa. Eur J Plant Pathol 135:127–135

    Article  Google Scholar 

  39. Simpson AJ, Reinach FC, Arruda P et al (2000) The genome sequence of the plant pathogen Xylella fastidiosa. Nature 406:151–159

    Article  PubMed  CAS  Google Scholar 

  40. Sun Q, Sun Y, Walker MA, Labavitch JM (2013) Vascular occlusions in grapevines with Pierce’s disease make disease symptom development worse. Plant Physiol 161:1529–1541

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  41. Van Sluys MA, de Oliveira MC, Monteiro-Vitorello CB et al (2003) Comparative analysis of the complete genome sequences of Pierce’s disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol 185:1018–1026

    Article  PubMed  PubMed Central  Google Scholar 

  42. Voegel TM, Warren JG, Matsumoto A, Igo MM, Kirkpatrick BC (2010) Localization and characterization of Xylella fastidiosa haemagglutinin adhesions. Microbiology 156:2172–2179

    Article  PubMed  CAS  Google Scholar 

  43. Wells JM, Raju BC, Hung H-Y, Weisberg WG, Mandeico-Paul L, Brenner DJ (1987) Xylella fastidiosa gen. Nov., sp. Nov: Gram-negative, xylem limited, fastidious plant bacteria related to Xanthomonas spp. Int J Sys Bacteriol 37:136–143

    Article  CAS  Google Scholar 

  44. Wulff NA, Mariano AG, Gaurivaud P, de Almeida Souza LC, Virgilio ACD, Monteiro PB (2008) Influence of culture medium pH on growth, aggregation and biofilm formation of Xylella fastidiosa. Curr Microbiol 57:127–132

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter C. Andersen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shriner, A.D., Andersen, P.C. Effect of Oxygen on the Growth and Biofilm Formation of Xylella fastidiosa in Liquid Media. Curr Microbiol 69, 866–873 (2014). https://doi.org/10.1007/s00284-014-0660-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-014-0660-2

Keywords

Navigation