Microbial Ecology

, Volume 58, Issue 1, pp 189–198 | Cite as

Bacterial Succession on the Leaf Surface: A Novel System for Studying Successional Dynamics

Plant Microbe Interactions


Succession is a widely studied process in plant and animal systems, but succession in microbial communities has received relatively little attention despite the ubiquity of microorganisms in natural habitats. One important microbial habitat is the phyllosphere, or leaf surface, which harbors large, diverse populations of bacteria and offers unique opportunities for the study of succession and temporal community assembly patterns. To explore bacterial community successional patterns, we sampled phyllosphere communities on cottonwood (Populus deltoides) trees multiple times across the growing season, from leaf emergence to leaf fall. Bacterial community composition was highly variable throughout the growing season; leaves sampled as little as a week apart were found to harbor significantly different communities, and the temporal variability on a given tree exceeded the variability in community composition between individual trees sampled on a given day. The bacterial communities clearly clustered into early-, mid-, and late-season clusters, with early- and late-season communities being more similar to each other than to the mid-season communities, and these patterns appeared consistent from year to year. Although we observed clear and predictable changes in bacterial community composition during the course of the growing season, changes in phyllosphere bacterial diversity were less predictable. We examined the species–time relationship, a measure of species turnover rate, and found that the relationship was fundamentally similar to that observed in plant and invertebrate communities, just on a shorter time scale. The temporal dynamics we observed suggest that although phyllosphere bacterial communities have high levels of phylogenetic diversity and rapid turnover rates, these communities follow predictable successional patterns from season to season.


  1. 1.
    Adler PB, Lauenroth W (2003) The power of time: spatiotemporal scaling of species diversity. Ecol Lett 6:749–756CrossRefGoogle Scholar
  2. 2.
    Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in-situ detection of individual microbial cells without cultivation. Microbiol Mol Biol Rev 59:143–169Google Scholar
  3. 3.
    Andrews JH, Harris RF (2000) The ecology and biogeography of microorganisms of plant surfaces. Annu Rev Phytopathol 38:145–180PubMedCrossRefGoogle Scholar
  4. 4.
    Chelius MK, Triplett EW (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microb Ecol 41:252–263PubMedGoogle Scholar
  5. 5.
    Ciferri O (1999) Microbial degradation of paintings. Appl Environ Microbiol 65:879–885PubMedGoogle Scholar
  6. 6.
    Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B Biol Sci 345:101–118PubMedCrossRefGoogle Scholar
  7. 7.
    Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310PubMedCrossRefGoogle Scholar
  8. 8.
    Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144CrossRefGoogle Scholar
  9. 9.
    Coppola S, Mauriello G, Aponte M, Moschetti G, Villani F (2000) Microbial succession during ripening of Naples-type salami, a southern Italian fermented sausage. Meat Sci 56:321–329CrossRefGoogle Scholar
  10. 10.
    DeSantis TZ, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006) NAST: a multiple sequence alignment server for comparative analysis of 16 S rRNA genes. Nucleic Acids Res 34:W394–W399PubMedCrossRefGoogle Scholar
  11. 11.
    DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072PubMedCrossRefGoogle Scholar
  12. 12.
    Ercolani GL (1991) Distribution of epiphytic bacteria on olive leaves and the influence of leaf age and sampling time. Microb Ecol 21:35–48CrossRefGoogle Scholar
  13. 13.
    Ercolini D, Mauriello G, Blaiotta G, Moschetti G, Coppola S (2004) PCR-DGGE fingerprints of microbial succession during a manufacture of traditional water buffalo mozzarella cheese. J Appl Microbiol 96:263–270PubMedCrossRefGoogle Scholar
  14. 14.
    Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10CrossRefGoogle Scholar
  15. 15.
    Favier CF, Vaughan EE, De Vos WM, Akkermans ADL (2002) Molecular monitoring of succession of bacterial communities in human neonates. Appl Environ Microbiol 68:219–226PubMedCrossRefGoogle Scholar
  16. 16.
    Fierer N, Jackson JA, Vigalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120PubMedCrossRefGoogle Scholar
  17. 17.
    van der Gast CJ, Ager D, Lilley AK (2008) Temporal scaling of bacterial taxa is influenced by both stochastic and deterministic ecological factors. Environ Microbiol 10:1411–1418PubMedCrossRefGoogle Scholar
  18. 18.
    Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347CrossRefGoogle Scholar
  19. 19.
    Hirano SS, Upper CD (1991) Bacterial community dynamics. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 271–294Google Scholar
  20. 20.
    Horner-Devine MC, Lage M, Hughes JB, Bohannan BJM (2004) A taxa-area relationship for bacteria. Nature 432:750–753PubMedCrossRefGoogle Scholar
  21. 21.
    Huston MA (1979) A general hypothesis of species diversity. Am Nat 113:81–101CrossRefGoogle Scholar
  22. 22.
    Huston MA (1994) Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge, UKGoogle Scholar
  23. 23.
    Jackson CR, Churchill PF, Roden EE (2001) Successional changes in bacterial assemblage structure during epilithic biofilm development. Ecology 82:555–566Google Scholar
  24. 24.
    Kadivar H, Stapleton AE (2003) Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb Ecol 45:353–361PubMedCrossRefGoogle Scholar
  25. 25.
    Kinkel L, Nordheim EV, Andrews JH (1992) Microbial community analysis in incompletely or destructively sampled systems. Microb Ecol 24:227–242CrossRefGoogle Scholar
  26. 26.
    Kinkel LL (1997) Microbial population dynamics on leaves. Ann Rev Phytopath 35:327–347CrossRefGoogle Scholar
  27. 27.
    Lambais MR, Crowley DE, Cury JC, Bull RC, Rodrigues RR (2006) Bacterial diversity in tree canopies of the Atlantic forest. Science 312:1917PubMedCrossRefGoogle Scholar
  28. 28.
    Li J, Helmerhorst E, Leone C, Troxler R, Yaskell T, Haffajee A, Socransky S, Oppenheim F (2004) Identification of early microbial colonizers in human dental biofilm. J Appl Microbiol 97:1311–1318PubMedCrossRefGoogle Scholar
  29. 29.
    Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883PubMedCrossRefGoogle Scholar
  30. 30.
    Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235PubMedCrossRefGoogle Scholar
  31. 31.
    Lyautey E, Jackson CR, Cayrou J, Rols J, Garabétian F (2005) Bacterial community succession in natural river biofilm assemblages. Microb Ecol 50:589–601PubMedCrossRefGoogle Scholar
  32. 32.
    Maddison WP, Slatkin M (1991) Null models for the number of evolutionary steps in a character on a phylogenetic tree. Evolution 45:1184–1197CrossRefGoogle Scholar
  33. 33.
    Martin AP (2002) Phylogenetic approaches for describing and comparing the diversity of microbial communities. Appl Environ Microbiol 68:3673–3682PubMedCrossRefGoogle Scholar
  34. 34.
    Martiny AC, Jorgensen TM, Albrechtsen H, Arvin E, Molin S (2003) Long-term succession of structure and diversity of a biofilm formed in a model drinking water distribution system. Appl Environ Microbiol 69:6899–6907PubMedCrossRefGoogle Scholar
  35. 35.
    Nakasaki K, Nag K, Karita S (2005) Microbial succession associated with organic matter decomposition during thermophilic composting of organic waste. Waste Manag Res 23:48–56PubMedCrossRefGoogle Scholar
  36. 36.
    Nemergut DR, Anderson SP, Cleveland CC, Martin AP, Miller AE, Seimon A, Schmidt SK (2007) Microbial community succession in an unvegetated, recently deglaciated soil. Microb Ecol 53:110–22PubMedCrossRefGoogle Scholar
  37. 37.
    Odum EP (1969) The strategy of ecosystem development. Science 164:262–270PubMedCrossRefGoogle Scholar
  38. 38.
    Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276:734–740PubMedCrossRefGoogle Scholar
  39. 39.
    Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177PubMedCrossRefGoogle Scholar
  40. 40.
    Peters S, Koschinsky S, Schwieger F, Tebbe CC (2000) Succession of microbial communities during hot composting as detected by PCR-single-strand-conformation polymorphism-based genetic profiles of small-subunit rRNA genes. Appl Environ Microbiol 66:930–936PubMedCrossRefGoogle Scholar
  41. 41.
    Petersen KM, Westall S, Jespersen L (2002) Microbial succession of Debaryomyces hansenii strains during the production of Danish surfaced-ripened cheeses. J Dairy Sci 85:478–486PubMedCrossRefGoogle Scholar
  42. 42.
    Preston F (1960) Time and space and the variation of species. Ecology 41:611–627CrossRefGoogle Scholar
  43. 43.
    Roberts DJ, Nica D, Zuo G, Davis JL (2002) Quantifying microbially induced deterioration of concrete: initial studies. Int Biodeterior Biodegrad 49:227–234CrossRefGoogle Scholar
  44. 44.
    Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge, UKGoogle Scholar
  45. 45.
    Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67PubMedCrossRefGoogle Scholar
  46. 46.
    Schloss PD, Handelsman J (2006) Introducing TreeClimber, a test to compare microbial community structures. Appl Environ Microbiol 72:2379–2384PubMedCrossRefGoogle Scholar
  47. 47.
    Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  48. 48.
    Thompson IP, Bailey MJ, Fenlon JS, Fermor TR, Lilley AK, Lynch JM, McCormack PJ, McQuilken MP, Purdy KJ, Rainey PB (1993) Quantitative and qualitative seasonal changes in the microbial community from the phyllosphere of sugar beet (Beta vulgaris). Plant Soil 150:177–191CrossRefGoogle Scholar
  49. 49.
    Webb CO, Ackerly DD, Kembel SW (2007) Phylocom: software for the analysis of community phylogenetic structure and character evolution. http://www.phylodiversity.net/phylocom
  50. 50.
    White EP (2004) Two-phase species–time relationships in North American land birds. Ecol Lett 7:329–336CrossRefGoogle Scholar
  51. 51.
    White EP, Adler PB, Lauenroth WK, Gill RA, Greenberg D, Kaufman DM, Rassweiler A, Rusak JA, Smith MD, Steinbeck JR, Waide RB, Yao J (2006) A comparison of the species–time relationship across ecosystems and taxonomic groups. Oikos 112:185–195CrossRefGoogle Scholar
  52. 52.
    Yang CH, Crowley DE, Borneman J, Keen NT (2001) Microbial phyllosphere populations are more complex than previously realized. Proc Natl Acad Sci USA 98:3889–3894PubMedCrossRefGoogle Scholar
  53. 53.
    Yu YN, Breitbart M, McNairnie P, Rohwer F (2006) FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7:57PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ColoradoBoulderUSA
  2. 2.Cooperative Institute for Research in Environmental SciencesUniversity of ColoradoBoulderUSA

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