Skip to main content
Log in

Exploring Biodiversity in the Bacterial Community of the Mediterranean Phyllosphere and its Relationship with Airborne Bacteria

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We studied the structure and diversity of the phyllosphere bacterial community of a Mediterranean ecosystem, in summer, the most stressful season in this environment. To this aim, we selected nine dominant perennial species, namely Arbutus unedo, Cistus incanus, Lavandula stoechas, Myrtus communis, Phillyrea latifolia, Pistacia lentiscus, Quercus coccifera (woody), Calamintha nepeta, and Melissa officinalis (herbaceous). We also examined the extent to which airborne bacteria resemble the epiphytic ones. Genotype composition of the leaf and airborne bacteria was analysed by using denaturing gradient gel electrophoresis profiling of a 16S rDNA gene fragment; 75 bands were cloned and sequenced corresponding to 28 taxa. Of these, two were found both in the air and the phyllosphere, eight only in the air, and the remaining 18 only in the phyllosphere. Only four taxa were found on leaves of all nine plant species. Cluster analysis showed highest similarity for the five evergreen sclerophyllous species. Aromatic plants were not grouped all together: the representatives of Lamiaceae, bearing both glandular and non-glandular trichomes, formed a separate group, whereas the aromatic and evergreen sclerophyllous M. communis was grouped with the other species of the same habit. The epiphytic communities that were the richest in bacterial taxa were those of C. nepeta and M. officinalis (Lamiaceae). Our results highlight the remarkable presence of lactic acid bacteria in the phyllosphere under the harsh conditions of the Mediterranean summer, the profound dissimilarity in the structure of bacterial communities in phyllosphere and air, and the remarkable differences of leaf microbial communities on neighbouring plants subjected to similar microbial inocula; they also point to the importance of the leaf glandular trichome in determining colonization patterns.

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.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Andrews JH (1992) Biological control in the phyllosphere. Annu Rev Phytopathol 30:603–635

    Article  PubMed  CAS  Google Scholar 

  2. Baldotto LEB, Olivares FL (2008) Phyloepiphytic interaction between bacteria and different plant species in a tropical agricultural system. Can J Microbiol 54:918–931

    Article  PubMed  CAS  Google Scholar 

  3. Bowers RM, McLetchie S, Knight R, Fierer N (2011) Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments. ISME J 5:601–612

    Article  PubMed  CAS  Google Scholar 

  4. Chalkos DG (2010) Effects of secondary metabolites of aromatic plants on the structure and metabolism of the soil microbial communities. PhD thesis. Aristotle University of Thessaloniki: Thessaloniki, Greece (in Greek with English summary)

  5. Constantinidou ΗΑ, Hirano SS, Baker LS, Upper CD (1990) Atmospheric dispersal of ice nucleation-active bacteria: the role of rain. Phytopathology 80:934–937

    Article  Google Scholar 

  6. de Jager ES, Wehner FC, Korsten L (2001) Microbial ecology of the mango phylloplane. Microb Ecol 42:201–207

    PubMed  Google Scholar 

  7. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Meringb C, Vorholta JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA 106:16428–16433

    Article  PubMed  CAS  Google Scholar 

  8. Fierer N, McCain CM, Meir P, Zimmermann M, Rapp JM, Silman MR, Knight R (2011) Microbes do not follow the elevation diversity patterns of plants and animals. Ecology 92:797–804

    Article  PubMed  Google Scholar 

  9. Karamanoli K, Vokou D, Menkissoglu O, Constantinidou HΙ (2000) Bacterial colonization of the phyllosphere of Mediterranean aromatic plants. J Chem Ecol 26:2035–2048

    Article  CAS  Google Scholar 

  10. Knief C, Ramette A, Frances L, Alonso-Blanco C, Vorholt JA (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J 4:719–728

    Article  PubMed  CAS  Google Scholar 

  11. Lambais MR, Crowley DE, Cury JC, Bull RC, Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917–1917

    Article  PubMed  CAS  Google Scholar 

  12. Lavermicocca P, Gobbetti M, Corsetti A, Caputo L (1998) Characterization of lactic acid bacteria isolated from olive phylloplane and table olive brines. Ital J Food Sci 10:27–39

    CAS  Google Scholar 

  13. Lindemann J, Constantinidou HΑ, Barchet WR, Upper CD (1982) Plants as sources of airborne bacteria, including ice nucleation-active bacteria. Appl Environ Microbiol 44:1059–1063

    PubMed  CAS  Google Scholar 

  14. Lindow SE (1996) Role of immigration and other processes in determining epiphytic bacterial populations: implications for disease management. In: Morris CE, Nicot PC, Nguyen C (eds) Aerial plant surface microbiology. Plenum, New York, pp 155–168

    Chapter  Google Scholar 

  15. Mariano RLR, McCarter SM (1993) Epiphytic survival of Pseudomonas viridiflava on tomato and selected weed species. Microb Ecol 26:47–58

    Article  Google Scholar 

  16. Mew TW, Vera Cruz CM (1986) Epiphytic colonization of host and non-host plants by phytopathogenic bacteria. In: Fokkema NJ, van den Heuvel J (eds) Microbiology of the phyllosphere. Cambridge University Press, New York, pp 269–282

    Google Scholar 

  17. Muller T, Behrendt U, Muller M (1996) Antagonistic activity in plant-associated lactic acid bacteria. Microbiol Res 151:63–70

    Article  Google Scholar 

  18. Mundt JO, Coggins JH, Johnson LF (1962) Growth of Streptococcus faecalis var. liquefaciens on plants. Appl Microbiol 10:552–555

    PubMed  CAS  Google Scholar 

  19. Muyzer G, Teske A, Wirsen CO, Jannasch HW (1995) Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Arch Microbiol 164:165–171

    Article  PubMed  CAS  Google Scholar 

  20. Pugh GJF, Buckley NJ (1971) The leaf surface as substrate for colonization by fungi. In: Preece TF, Dickinson CH (eds) Ecology of leaf surface micro-organisms. Academic, London, pp 431–445

    Google Scholar 

  21. Quaiser A, Ochsenreiter T, Lanz C, Schuster SC, Treusch AH, Eck J, Schleper C (2003) Acidobacteria form a coherent but highly diverse group within the bacterial domain: evidence from environmental genomics. Mol Microbiol 50:563–575

    Article  PubMed  CAS  Google Scholar 

  22. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893

    Article  PubMed  Google Scholar 

  23. Schönherr J, Baur P (1996) Cuticle permeability studies: a model for estimating leaching of plant metabolites to leaf surfaces. In: Morris CE, Nicot PC, Nguyen C (eds) Aerial plant surface microbiology. Plenum, New York, pp 1–23

    Chapter  Google Scholar 

  24. Sokal R, Michener C (1958) A statistical method for evaluating systematic relationships. Univ Kans Sci Bull 38:1409–1438

    Google Scholar 

  25. Vareli K, Briasoulis E, Pilidis G, Sainis I (2009) Molecular confirmation of Planktothrix rubescens as the cause of intense, microcystin-synthesizing cyanobacterial bloom in Lake Ziros, Greece. Harmful Algae 8:447–453

    Article  CAS  Google Scholar 

  26. Vokou D (2007) Allelochemicals, allelopathy and essential oils: a field in search of definitions and structure. Allelopathy J 19:119–135

    Google Scholar 

  27. Vokou D, Chalkos D, Karamanoli K (2006) Microorganisms and allelopathy: a one-sided approach. In: Reigosa MJ, Pedrol N, Gonzalez L (eds) Allelopathy: a physiological process with ecological implications. Springer, Dordrecht, pp 341–371

    Google Scholar 

  28. Vokou D, Margaris NS (1988) Decomposition of terpenes by soil microorganisms. Pedobiologia 31:413–419

    CAS  Google Scholar 

  29. Vokou D, Margaris NS, Lynch JM (1984) Effects of volatile oils from aromatic shrubs on soil microorganisms. Soil Biol Biochem 16:509–513

    Article  CAS  Google Scholar 

  30. Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755

    Article  PubMed  CAS  Google Scholar 

  31. Yadav RKP, Bosabalidis AM, Vokou D (2004) Leaf structural features of Mediterranean perennial species: plasticity and life form specificity. J Biol Res 2:21–34

    Google Scholar 

  32. Yadav RKP, Halley JM, Karamanoli K, Constantinidou HI, Vokou D (2004) Bacterial populations on the leaves of Mediterranean plants: quantitative features and testing of distribution models. Environ Exp Bot 52:63–77

    Article  Google Scholar 

  33. Yadav RKP, Karamanoli K, Vokou D (2011) Bacterial populations on the phyllosphere of Mediterranean plants: influence of leaf age and leaf surface. Front Agr China 5:60–63

    Article  Google Scholar 

  34. Yadav RKP, Karamanoli K, Vokou D (2005) Bacterial colonization of the phyllosphere of Mediterranean perennial species as influenced by leaf structural and chemical features. Microb Ecol 50:185–196

    Article  PubMed  CAS  Google Scholar 

  35. Yadav RKP, Papatheodorou EM, Karamanoli K, Constantinidou H-IA, Vokou D (2008) Abundance and diversity of the phyllosphere bacterial communities of Mediterranean perennial plants that differ in leaf chemistry. Chemoecology 18:217–226

    Article  CAS  Google Scholar 

  36. Yang CH, Crowley DE, Borneman J, Keen NT (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci USA 98:3889–3894

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Prof. S. E. Lindow, University of California, Berkeley, for his constructive comments on an earlier version of our manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Despoina Vokou.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vokou, D., Vareli, K., Zarali, E. et al. Exploring Biodiversity in the Bacterial Community of the Mediterranean Phyllosphere and its Relationship with Airborne Bacteria. Microb Ecol 64, 714–724 (2012). https://doi.org/10.1007/s00248-012-0053-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0053-7

Keywords

Navigation