Skip to main content
SpringerLink
Log in

Life on a Leaf: Bacterial Epiphytes of a Salt-Excreting Desert Tree

  • Chapter
  • First Online:
Symbioses and Stress

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 17))

Abstract

The surfaces of aboveground parts of plants – the phyllosphere – are normally colonized by a variety of bacteria, yeasts, and fungi (Lindow and Leveau, 2002). Bacteria are the most numerous colonists of leaves, often being found in numbers averaging 106–107 cells/cm2 of leaf (Andrews and Harris, 2000; Beattie and Lindow, 1995; Hirano and Upper, 1989). In spite of their worldwide distribution (Morris and Kinkel, 2002), studies of the composition of bacterial communities on leaves have been relatively limited in scope, mostly focusing on potential pathogens of agriculturally relevant plants (Beattie and Lindow, 1994; Dik, et al., 1992; Ercolani, 1991).

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 299.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 379.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 379.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Amman, R., Fuchs, B.M. and Behrens, S. (2001) The identification of microorganisms by fluorescence in situ hybridization. Curr. Opin. Biotechnol. 12: 231–236.

    Article  Google Scholar 

  • Andrews, J.H. and Harris, R.F. (2000) The ecology and biogeography of microorganisms on plant surfaces. Annu. Rev. Phytopathol. 38: 145–180.

    Article  PubMed  Google Scholar 

  • Beattie, G.A. and Lindow, S.E. (1994) Survival, growth, and localization of epiphytic fitness mutants of Pseudomonas syringae on leaves. Appl. Environ. Microbiol. 60: 3790–3798.

    PubMed  CAS  Google Scholar 

  • Beattie, G.A. and Lindow, S.E. (1995) The secret life of foliar bacterial pathogens on leaves. Annu. Rev. Phytopathol. 33: 145–172.

    Article  PubMed  CAS  Google Scholar 

  • Brandl, M.T. and Mandrell, R.E. (2002) Fitness of Salmonella enterica serovar Thompson in the cilantro phyllosphere. Appl. Environ. Microbiol. 68: 3614–3621.

    Article  PubMed  CAS  Google Scholar 

  • Brock, J.H. (1994) Tamarix spp. (Salt Cedar), an invasive exotic woody plant in arid and semi- arid riparian habitats of western USA, In: L.C. de Waal, L.E. Child, P.M. Wade and J.H. Brock (eds.) Ecology and Management of Invasive Riverside Plants. Wiley, New York, pp. 27–44.

    Google Scholar 

  • Corpe, W.A. and Rheem, S. (1989) Ecology of the methylotrophic bacteria on leaving leaf surfaces. FEMS Microbiol. Ecol. 62: 243–250.

    Article  CAS  Google Scholar 

  • Curtis, T.P., Sloan, W.T. and Scannell, J.W. (2002) Estimating prokaryotic diversity and its limits. Proc. Natl. Acad. Sci. USA 99: 10494–10499.

    Article  PubMed  CAS  Google Scholar 

  • Dik, A.J., Fokkema, N.J. and Van Pelt, A. (1992) Influence of climatic and nutritional factors on yeast population dynamics in the phyllopshere of wheat. Microb. Ecol. 23: 41–52.

    Article  Google Scholar 

  • Edwards, I.P., Burgmann, H., Miniaci, C. and Zeyer, J. (2006) Variation in microbial community composition and culturability in the rhizosphere of Leucanthemopsis alpina (L.) Heywood and adjacent bare soil along an alpine chronosequence. Microb. Ecol. 52: 679–692.

    Article  PubMed  CAS  Google Scholar 

  • Ercolani, G.L. (1991) Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microbial. Ecol. 21: 35–48.

    Article  Google Scholar 

  • Euzéby, J.P. (2006) List of Prokaryotic Names with Standing in Nomenclature – Genus Halomonas. http://www.bacterio.cict.fr/h/halomonas.html

  • Facciola, S. (1990) Cornucopia II: A Source Book of Edible Plants, 2nd ed, Kampong, Vista, CA.

    Google Scholar 

  • Feinbrun-Dothan, N. (1972) Flora Palaestina, part 3: Ericaceae to compositae. Israel Academy of Science and Humanities, Jurusalem, pp. 1240.

    Google Scholar 

  • Fürnkranz, M., Wanek, W., Richter, A., Abell, G., Rasche, F. and Sessitsch, A. (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 

  • Garcia, M.T., Ventosa, A. and Mellado, E. (2005) Catabolic versatility of aromatic compound-­degrading halophilic bacteria. FEMS Microbiol. Ecol. 54: 97–109.

    Article  PubMed  CAS  Google Scholar 

  • Hirano, S.S. and Upper, C.D. (1989) Diel variation in population size and ice nucleation activity of Pseudomonas syringae on snap bean leaflets. Appl. Environ. Microbiol. 55: 623–630.

    PubMed  CAS  Google Scholar 

  • Hirano, S.S. and Upper, C.D. (1991) Bacterial community dynamics, In: J.H. Andrews and S.S. Hirano (eds.) Microbial Ecology of Leaves. Springer, New York, pp. 271–294.

    Chapter  Google Scholar 

  • Hirano, S.S. and Upper, C.D. (1995) Ecology of ice nucleation-active bacteria, In: R.E. Lee, Jr., G.J. Warren and L.V. Gusta (eds.) Biological Ice Nucleation and Its Applications. American Phytological Society, St. Paul, MN, pp. 41–61.

    Google Scholar 

  • Hughes, J.B., Hellmann, J.J., Ricketts, T.H. and Bohannan B.J. (2001) Counting the uncountable: ­statistical approaches to estimating microbial diversity. Appl. Environ. Microbiol. 67: 4399–4406.

    Article  PubMed  CAS  Google Scholar 

  • Jacobs, J.L. and Sundin, G.W. (2001) Effect of solar UV-B radiation on a phyllosphere bacterial community. Appl. Environ. Microbiol. 67: 5488–5496.

    Article  PubMed  CAS  Google Scholar 

  • Jacobs, J.L., Carroll, T.L. and Sundin, G.W. (2005) The role of pigmentation, ultraviolet radiation ­tolerance, and leaf colonization strategies in the epiphytic survival of phyllosphere bacteria. Microbial Ecol. 49: 104–113.

    Article  CAS  Google Scholar 

  • Jurkevitch, E.J. and Shapira, G. (2000) Structure and colonization dynamics of epiphytic bacterial communities and of selected component strains on tomato (Lycopersicon esculentum) leaves. Microbial Ecol. 40: 300–308.

    Google Scholar 

  • Kampfer, P., Ruppel, S. and Remus, R. (2005) Enterobacter radicincitans sp. nov., a plant growth ­promoting species of the family Enterobacteriaceae. Syst. Appl. Microbiol. 28: 213–221.

    Article  PubMed  Google Scholar 

  • Kemp, P.F. and Aller J.Y. (2004) Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol. Ecol. 47: 161–177.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy, M.J., Reader, S.L. and Swierczynski, L.M. (1994) Preservation records of micro-organisms: evidence of the tenacity of life. Microbiology 140: 2513–2529.

    Article  PubMed  Google Scholar 

  • Kinkel, L.L., Wilson, M. and Lindow, S.E. (2000) Plant species and plant incubation conditions influence variability in epiphytic bacterial population size. Microbial Ecol. 39:1–11.

    Article  Google Scholar 

  • Lambais, M.R., Crowley, D.E., Cury, J.C., Bull, R.C. and Rodrigues, R.R. (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312: 1917.

    Article  PubMed  CAS  Google Scholar 

  • Leibowitz, J. (1944) Isolation of Trehalose from Desert Manna. Biochem. J. 38: 205–206.

    PubMed  CAS  Google Scholar 

  • Lindow, S.E. and Brandl, M.T. (2003) Microbiology of the phyllosphere. Appl. Environ. Microbiol. 69: 1875–1883.

    Article  PubMed  CAS  Google Scholar 

  • Lindow, S.E. and Leveau, J.H.J. (2002) Phyllosphere microbiology. Curr. Opini. Biotechnol. 13: 238–243.

    Article  CAS  Google Scholar 

  • Llamas, I., del Moral, A., Martinez-Checa, F., Arco, Y., Arias, S. and Quesada, E. (2006) Halomonas maura is a physiologically versatile bacterium of both ecological and biotechnological interest. Antonie Van Leeuwenhoek 89: 395–403.

    Article  PubMed  CAS  Google Scholar 

  • Madigan, M.T. and Oren A. (1999) Thermophilic and halophilic extremophiles. Curr. Opin. Microbiol. 2: 265–2699.

    Article  PubMed  CAS  Google Scholar 

  • Mata, J.A., Martinez-Canovas, J., Quesada, E. and Bejar, V. (2002) A detailed phenotypic characterization of the type strains of Halomonas species. Syst. Appl. Microbiol. 25: 360–375.

    Article  PubMed  CAS  Google Scholar 

  • Morris, C.E. and Kinkel, L. (2002) Fifty years of phyllosphere microbiology: Significant contributions to research in related fields, In: S.E. Lindow, E.I. Hecht-Poinar and V. Elliott (eds.) Phyllosphere Microbiology. APS Press, St. Paul, MN, pp. 365–375.

    Google Scholar 

  • Muyzer, G., de Waal E.C. and Uitterlinden A.G. (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 

  • O’Brien, R.D. and Lindow, S.E. (1989) Effect of plant species and environmental conditions on epiphytic population sizes of Pseudomonas syringae and other bacteria. Phytopathol. 79: 619–627.

    Article  Google Scholar 

  • Ott, E.M., Muller, T., Muller, M., Franz, C.M., Ulrich, A., Gabel, M. and Seyfarth, W. (2001) Population dynamics and antagonistic potential of enterococci colonizing the phyllosphere of grasses. J. Appl. Microbiol. 91: 54–66.

    Article  PubMed  CAS  Google Scholar 

  • Qvit-Raz, N., Jurkevitch, E. and Belkin, S. (2008) Drop-size soda lakes: transient microbial habitats on a salt-secreting desert tree. Genetics. 178: 1615–1622.

    Google Scholar 

  • Ravenschlag, K., Sahm, K., Pernthaler, J. and Amann, R. (1999) High bacterial diversity in permanently cold marine sediments. Appl. Environ. Microbiol. 65: 3982–3989.

    PubMed  CAS  Google Scholar 

  • Ruinen, J. (1975) Nitrogen fixation in the phyllosphere, In: W.D.P. Stewart (ed.) Nitrogen Fixation by Free-Living Microorganisms. Cambridge University Press, Cambridge, pp. 85–100.

    Google Scholar 

  • Schloss, P.D. and Handelsman, J. (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol. 71: 1501–1506.

    Article  PubMed  CAS  Google Scholar 

  • Simon, R.D., Abeliovich, A. and Belkin, S. (1994) A novel terrestrial halophilic environment: The phylloplane of Atriplex halimus, a salt-excreting plant. FEMS Microbiol. Ecol. 14: 99–109.

    Article  Google Scholar 

  • Sogin, M.L., Morrison, H.G., Huber, J.A., Welch, D.M, Huse S.M., Neal, P.R., Arrieta, J.M. and Herndl, G.J. (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc. Natl. Acad. Sci. USA 103: 12115–12120.

    Article  PubMed  CAS  Google Scholar 

  • Stout, J.D. (1960a) Bacteria of soil and pasture leaves at Claudelands showgrounds. N. Z. J. Agr. Res. 3: 413–430.

    Article  Google Scholar 

  • Stout, J.D. (1960b) Biological studies of some tussock-grassland soils. N. Z. J. Agr. Res. 3: 214–223.

    Article  Google Scholar 

  • Sundin, G.W. and Jacobs, J.L. (1999) Ultraviolet radiation (UVR) sensitivity analysis and UVR survival strategies of a bacterial community from the phyllosphere of field-grown peanut (Arachis hypogeae L.). Microb. Ecol. 38: 27–38.

    Article  PubMed  Google Scholar 

  • Sundin G.W. and Murillo, J. (1999) Functional analysis of the Pseudomonas syringae rulAB determinant in tolerance to ultraviolet B (290–320 nm) radiation and distribution of rulAB among P. syringae pathovars. Environ. Microbiol. 1: 75–87.

    Article  PubMed  CAS  Google Scholar 

  • Sundin, G.W., Kidambi, S.P., Ullrich, M. and Bender, C.L. (1996) Resistance to ultraviolet light in Pseudomonas syringae: sequence and functional analysis of the plasmid-encoded rulAB genes. Gene 177: 77–81.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, I.P., Bailey, M.J., Fenlon, J.S., Fermor, T.R., Lilley, A.K., Lynch, J.M., McCormack, P.J., McQuilken, M.P. and Purdy, K.J. (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 

  • Thomson, W.W., Berry, W.L. and Liu, L.L. (1969) Localization and secretion of salt by the salt glands of Tamarix aphylla. Proc. Natl. Acad. Sci. USA 63: 310–317.

    Article  PubMed  CAS  Google Scholar 

  • Waisel, Y. (1961) Ecological studies on Tamarix aphylla (L.) Karst. III. The salt economy. Plant Soil 13: 356–364.

    Article  CAS  Google Scholar 

  • Waisel, Y. (1991) The glands of Tamarix aphylla: a system for salt secretion or for carbon concentration? Physiol. Plant 83: 506.

    Article  CAS  Google Scholar 

  • Wolkers, W.F., Tablin, F. and Crowe J.H. (2002) From anhydrobiosis to freeze-drying of eukaryotic cells. Comp. Biochem. Physiol. Part A. 131: 535–543.

    Article  Google Scholar 

  • Yang, C.-H., Crowley, D.E., Borneman, J. and Keen, N.T. (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

Author information

Authors and Affiliations

  1. Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, 91904, Israel

    Shimshon Belkin & Noga Qvit-Raz

Authors
  1. Shimshon Belkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Noga Qvit-Raz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shimshon Belkin .

Editor information

Editors and Affiliations

  1. University of Jerusalem, Mevo Hadas 20, Efrat, 90435, Israel

    Joseph Seckbach

  2. , Institute of Plant Sciences, Karl-Franzens-University, Holteigasse 6, Graz, 8010, Austria

    Martin Grube

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Belkin, S., Qvit-Raz, N. (2010). Life on a Leaf: Bacterial Epiphytes of a Salt-Excreting Desert Tree. In: Seckbach, J., Grube, M. (eds) Symbioses and Stress. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 17. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9449-0_19

Download citation

Publish with us

Policies and ethics

Search

Navigation