Skip to main content

Advertisement

SpringerLink
Log in

Variability of Bacterial Community Composition on Leaves Between and Within Plant Species

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The phyllosphere is one of the largest habitats for terrestrial microorganisms. To gain a better insight into the factors underlying the composition of bacterial communities inhabiting leaf surfaces we performed culture-dependent and independent (Denaturing Gradient Gel Electrophoresis) analyses on the bacteria associated with the leaves of three plant species: Amygdalus communis, Citrus paradisi, and Nicotiana glauca. We found that the culturable classes Bacilli and Actinobacteria were the predominant classes on the phyllosphere of all three plant species. In contrast to this consistency on the bacterial class level, we found a significant variation on the bacterial species-level based on the culturable methods. Although some variation was detected among individual plants within one plant species, the inter-specific variability exceeded the intra-specific variability. C. paradisi leaf surface had the highest predicted total species richness (Chao 2 and ICE) and the highest species diversity (βw) among the three plant species. Our findings demonstrate that environmental conditions, mainly the plant species within a site, govern the bacterial community composition on leaf surfaces.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Baas-Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. WP Van Stockum & Zoon, The Hague

    Google Scholar 

  2. Lindström ES, Langenheder S (2011) Local and regional factors influencing bacterial community assembly. Environ Microbiol Rep 4:1–9

    Article  Google Scholar 

  3. Halpern M, Raats D, Lev-Yadun S (2007) Plant biological warfare: infecting pathogenic bacteria into herbivores by thorns. Environ Microbiol 9:584–592

    Article  PubMed  CAS  Google Scholar 

  4. Halpern M, Raats D, Lev-Yadun S (2007) The potential antiherbivory role of microorganisms on plant thorns. Plant Signal Behav 2:503–504

    Article  PubMed  Google Scholar 

  5. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    Article  PubMed  CAS  Google Scholar 

  6. Lindow SE, Leveau JH (2002) Phyllosphere microbiology. Curr Opin Biotechnol 13:238–243

    Article  PubMed  CAS  Google Scholar 

  7. 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 

  8. Junker RR, Loewel C, Gross R et al (2011) Composition of epiphytic bacterial communities differs on petals and leaves. Plant Biol 13:918–924

    Article  PubMed  CAS  Google Scholar 

  9. 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 

  10. Delmotte N, Knief C, Chaffron S et al (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci USA 106:16428–16433

    Article  PubMed  CAS  Google Scholar 

  11. Fürnkranz M, Wanek W, Richter A et al (2008) Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2:561–570

    Article  PubMed  Google Scholar 

  12. Kim M, Singh D, Lai-Hoe A et al (2012) Distinctive phyllosphere bacterial communities in tropical trees. Microb Ecol 63:674–681

    Article  PubMed  Google Scholar 

  13. 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 

  14. Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S (2011) Phyllosphere microbial communities of a salt-excreting desert tree: geographical location determines population structure. Appl Environ Microbiol 7:7647–7655

    Article  Google Scholar 

  15. Rasche F, Marco-Noales E, Velvis H et al (2006) Structural characteristics and plant-beneficial effects of bacteria colonizing the shoots of field grown conventional and genetically modified T4-lysozyme producing potatoes. Plant Soil 289:123–140

    Article  CAS  Google Scholar 

  16. van Overbeek L, van Elsas JD (2008) Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiol Ecol 64:283–296

    Article  PubMed  Google Scholar 

  17. Felske A, Rheims H, Wolterink A, Stackebrandt E, Akkermans AD (1997) Ribosome analysis reveals prominent activity of an uncultured member of the class Actinobacteria in grassland soils. Microbiology 143:2983–2989

    Article  PubMed  CAS  Google Scholar 

  18. Chun J, Lee JH, Jung Y et al (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261

    Article  PubMed  CAS  Google Scholar 

  19. Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700

    PubMed  CAS  Google Scholar 

  20. Rosef O, Kapperud G, Lauwers S, Gondrosen B (1985) Serotyping of Campylobacter-jejuni, Campylobacter coli and Campylobacter-lardis from domestic and wild animals. Appl Environ Microbiol 49:1507–1510

    PubMed  CAS  Google Scholar 

  21. Chao A, Shen TJ (2010) Program SPADE (Species Prediction and Diversity Estimation). Program and User’s Guide. http://chao.stat.nthu.edu.tw

  22. Magurran AE (2004) Measuring biological diversity. Blackwell Publishing, Oxford

    Google Scholar 

  23. Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples, version 7.52. User’s Guide and application published online. http://viceroy.eeb.uconn.edu/estimates

  24. Koleff P, Gaston KJ, Lennon JJ (2003) Measuring beta diversity for presence–absence data. J Anim Ecol 72:367–382

    Article  Google Scholar 

  25. Whittaker RH (1960) Vegetation of the Siskiyou Mountains, Oregon and California. Ecol Monogr 30:279–338

    Article  Google Scholar 

  26. ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector method for multivariate direct gradient analysis. Ecology 67:1167–1179

    Article  Google Scholar 

  27. 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 

  28. Halpern M, Waissler A, Dror A, Lev-Yadun S (2011) Biological warfare of the spiny plant: introducing pathogenic microorganisms into Herbivore’s tissues. Adv Appl Microbiol 74:97–116

    Article  PubMed  CAS  Google Scholar 

  29. Krimm U, Abanda-Nkpwatt D, Schwab W, Schreiber L (2005) Epiphytic microorganisms on strawberry plants (Fragaria ananassa cv. Elsanta): identification of bacterial isolates and analysis of their interaction with leaf surfaces. FEMS Microbiol Ecol 53:483–492

    Article  PubMed  CAS  Google Scholar 

  30. Thompson IP, Bailey MJ, Fenlon JS et al (1993) Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar-beet (Beta vulgaris). Plant Soil 150:177–191

    Article  Google Scholar 

  31. Brighigna L, Montaini P, Favilli F, Trejo AC (1992) Role of the nitrogen-fixing bacterial microflora in the epiphytism of Tillandsia (Bromeliaceae). Am J Bot 79:723–727

    Article  Google Scholar 

  32. Lindow SE, Arny DC, Upper CD (1978) Distribution of ice nucleation-active bacteria on plants in nature. Appl Environ Microbiol 36:831–838

    PubMed  CAS  Google Scholar 

  33. Corpe WA, Rheem S (1989) Ecology of the methylotrophic bacteria on living leaf surfaces. FEMS Microbiol Ecol 62:243–250

    Article  CAS  Google Scholar 

  34. Hirano SS, Upper CD (2000) Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae—a pathogen, ice nucleus, and epiphyte. Microbiol Mol Biol Rev 64:624–653

    Article  PubMed  CAS  Google Scholar 

  35. Opelt K, Berg C, Schonmann S, Eberl L, Berg G (2007) High specificity but contrasting biodiversity of Sphagnum-associated bacterial and plant communities in bog ecosystems independent of the geographical region. ISME J 1:502–516

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  37. Ruppel S, Krumbein A, Schreiner M (2008) Composition of the phyllospheric microbial populations on vegetable plants with different glucosinolate and carotenoid compositions. Microb Ecol 56:364–372

    Article  PubMed  CAS  Google Scholar 

  38. Hallman J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    Article  Google Scholar 

  39. Saitoh F, Noma M, Kawashima N (1985) The alkaloid contents of sixty Nicotiana species. Phytochemistry 24:477–480

    Article  CAS  Google Scholar 

  40. Kretschmar JA, Baumann TW (1999) Caffeine in Citrus flowers. Phytochemistry 52:19–23

    Article  CAS  Google Scholar 

  41. London-Shafir I, Shafir S, Eisikowitch D (2003) Amygdalin in almond nectar and pollen-facts and possible roles. Plant Syst Evol 238:87–95

    Google Scholar 

  42. Athayde ML, Coelho GC, Schenkel EP (2000) Caffeine and theobromine in epicuticular wax of Ilex paraguariensis A. St.-Hil. Phytochemistry 55:853–857

    Article  PubMed  CAS  Google Scholar 

  43. Bednarerk P, Osbourn A (2009) Plant-microbe interactions: chemical diversity in plant defense. Science 324:746–748

    Article  Google Scholar 

  44. Chen C, Li X, Yang J, Gong X, Li B, Zhang K (2008) Isolation of nicotine-degrading bacterium Pseudomonas sp. Nic22, and its potential application in tobacco processing. Int Biodeter Biodegr 62:226–231

    Article  CAS  Google Scholar 

  45. Zakaria ZA, Fatimah CA, Mat Jais AM et al (2006) The in vitro antibacterial activity of Muntingia calabura extracts. Int J Pharm 2:439–442

    Article  Google Scholar 

  46. Mazzafera P (2002) Degradation of caffeine by microorganisms and potential use of decaffeinated coffee husk and pulp in animal feeding. Sci Agric 59:815–821

    Article  CAS  Google Scholar 

  47. Ibrahim SA, Salameh MM, Phetsomphou S, Yang H, Seo CW (2006) Application of caffeine, 1,3,7- trimethylxanthine, to control Escherichia coli O157:H7. Food Chem 99:645–650

    Article  CAS  Google Scholar 

  48. Wang X, Liu Z, Ma H, Liu Z (2008) Screening of amygdalin-degrading microorganisms and relevant antagonistic microorganisms from peach rhizosphere soil. Acta Hortic 764:145–150

    Google Scholar 

  49. Mengoni A, Pini F, Huang LN, Shu WS, Bazzicalupo M (2009) Plant-by-plant variations of bacterial communities associated with leaves of the nickel hyperaccumulator Alyssum bertolonii Desv. Microb Ecol 58:660–667

    Article  PubMed  CAS  Google Scholar 

  50. Meyer KM, Leveau JHJ (2012) Microbial of the phyllosphere: a playground for testing ecological concepts. Oecologia 168:621–629

    Article  PubMed  Google Scholar 

  51. Lv D, Ma A, Bai Z, Zhuang X, Zhuang G (2012) Response of leaf-associated bacterial communities to primary acyl-homoserine lactone in the tobacco phyllosphere. Res Microbiol 163:24–119

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant from the Israel Science Foundation (ISF, Grant Nos. 189/08 and 1094/12).

Author information

Authors and Affiliations

  1. Department of Evolutionary and Environmental Biology, Faculty of Natural Sciences, University of Haifa, Mount Carmel, 31905, Haifa, Israel

    Ido Izhaki, Svetlana Fridman, Yoram Gerchman & Malka Halpern

  2. Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa, Oranim, 36006, Tivon, Israel

    Yoram Gerchman & Malka Halpern

Authors
  1. Ido Izhaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Svetlana Fridman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoram Gerchman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Malka Halpern
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ido Izhaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Izhaki, I., Fridman, S., Gerchman, Y. et al. Variability of Bacterial Community Composition on Leaves Between and Within Plant Species. Curr Microbiol 66, 227–235 (2013). https://doi.org/10.1007/s00284-012-0261-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00284-012-0261-x

Keywords

Search

Navigation