Microbial Ecology

, Volume 64, Issue 4, pp 1018–1027 | Cite as

Distinctive Bacterial Communities in the Rhizoplane of Four Tropical Tree Species

  • Yoon Myung Oh
  • Mincheol Kim
  • Larisa Lee-Cruz
  • Ang Lai-Hoe
  • Rusea Go
  • N. Ainuddin
  • Raha Abdul Rahim
  • Noraini Shukor
  • Jonathan M. Adams
Plant Microbe Interactions


It is known that the microbial community of the rhizosphere is not only influenced by factors such as root exudates, phenology, and nutrient uptake but also by the plant species. However, studies of bacterial communities associated with tropical rainforest tree root surfaces, or rhizoplane, are lacking. Here, we analyzed the bacterial community of root surfaces of four species of native trees, Agathis borneensis, Dipterocarpus kerrii, Dyera costulata, and Gnetum gnemon, and nearby bulk soils, in a rainforest arboretum in Malaysia, using 454 pyrosequencing of the 16S rRNA gene. The rhizoplane bacterial communities for each of the four tree species sampled clustered separately from one another on an ordination, suggesting that these assemblages are linked to chemical and biological characteristics of the host or possibly to the mycorrhizal fungi present. Bacterial communities of the rhizoplane had various similarities to surrounding bulk soils. Acidobacteria, Alphaproteobacteria, and Betaproteobacteria were dominant in rhizoplane communities and in bulk soils from the same depth (0–10 cm). In contrast, the relative abundance of certain bacterial lineages on the rhizoplane was different from that in bulk soils: Bacteroidetes and Betaproteobacteria, which are known as copiotrophs, were much more abundant in the rhizoplane in comparison to bulk soil. At the genus level, Burkholderia, Acidobacterium, Dyella, and Edaphobacter were more abundant in the rhizoplane. Burkholderia, which are known as both pathogens and mutualists of plants, were especially abundant on the rhizoplane of all tree species sampled. The Burkholderia species present included known mutualists of tropical crops and also known N fixers. The host-specific character of tropical tree rhizoplane bacterial communities may have implications for understanding nutrient cycling, recruitment, and structuring of tree species diversity in tropical forests. Such understanding may prove to be useful in both tropical forestry and conservation.

Supplementary material

248_2012_82_MOESM1_ESM.doc (164 kb)
ESM 1(DOC 164 kb)


  1. 1.
    Brodie E, Edwards S, Clipson N (2002) Bacterial community dynamics across a floristic gradient in a temperate upland grassland ecosystem. Microbial Ecol 44:260–270CrossRefGoogle Scholar
  2. 2.
    Fang CW, Radosevich M, Fuhrmann JJ (2001) Characterization of rhizosphere microbial community structure in five similar grass species using FAME and BIOLOG analyses. Soil Biol Biochem 33:679–682CrossRefGoogle Scholar
  3. 3.
    Broughton LC, Gross KL (2000) Patterns of diversity in plant and soil microbial communities along a productivity gradient in a Michigan old-field. Oecologia 125:420–427CrossRefGoogle Scholar
  4. 4.
    Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PG, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie van Leeuwenhoek 81:509–520PubMedCrossRefGoogle Scholar
  5. 5.
    McCaig AE, Glover LA, Prosser JI (2001) Numerical analysis of grassland bacterial community structure under different land management regimens by using 16S ribosomal DNA sequence data and denaturing gradient gel electrophoresis banding patterns. Appl Environ Microbiol 67:4554–4559PubMedCrossRefGoogle Scholar
  6. 6.
    Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378CrossRefGoogle Scholar
  7. 7.
    Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microb 67:4742–4751CrossRefGoogle Scholar
  8. 8.
    Wieland G, Neumann R, Backhaus H (2001) Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67:5849–5854PubMedCrossRefGoogle Scholar
  9. 9.
    Dunfield KE, Germida JJ (2003) Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically modified canola (Brassica napus). Appl Environ Microbiol 69:7310–7318PubMedCrossRefGoogle Scholar
  10. 10.
    van Elsas JD, Speksnijder AJ, van Overbeek LS (2008) A procedure for the metagenomics exploration of disease-suppressive soils. J Microbiol Methods 75:515–522PubMedCrossRefGoogle Scholar
  11. 11.
    Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445CrossRefGoogle Scholar
  12. 12.
    Buckley DH, Schmidt TM (2003) Diversity and dynamics of microbial communities in soils from agro-ecosystems. Environ Microbiol 5:441–452PubMedCrossRefGoogle Scholar
  13. 13.
    Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl Environ Microbiol 69:1800–1809PubMedCrossRefGoogle Scholar
  14. 14.
    Johnson MJ, Lee KY, Scow KM (2003) DNA fingerprinting reveals links among agricultural crops, soil properties, and the composition of soil microbial communities. Geoderma 114:279–303CrossRefGoogle Scholar
  15. 15.
    DiCello F, Bevivino A, Chiarini L, Fani R, Paffetti D, Tabacchioni S, Dalmastri C (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl Environ Microbiol 63:4485–4493Google Scholar
  16. 16.
    Uroz S, Calvaruso C, Turpaul MP, Pierrat JC, Mustin C, Frey-Klett P (2007) Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil. Appl Environ Microbiol 73:3019–3027PubMedCrossRefGoogle Scholar
  17. 17.
    Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252:169–175CrossRefGoogle Scholar
  18. 18.
    Nieto KF, Frankenberger WT (1989) Biosynthesis of cytokinins in soil. Soil Sci Soc Am J 53:735–740CrossRefGoogle Scholar
  19. 19.
    Hamdan H, Weller DM, Thomashow LS (1991) Relative importance of fluorescent siderophores and other factors in biological-control of Gaeumannomyces graminis var tritici by Pseudomonas fluorescens 2-79 and M4-80r. Appl Environ Microbiol 57:3270–3277PubMedGoogle Scholar
  20. 20.
    Berg G, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2005) Impact of plant species and site on rhizosphere-associated fungi antagonistic to Verticillium dahliae Kleb. Appl Environ Microbiol 71:4203–4213PubMedCrossRefGoogle Scholar
  21. 21.
    Marilley L, Aragno M (1999) Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots. Appl Soil Ecol 13:127–136CrossRefGoogle Scholar
  22. 22.
    Marilley L, Vogt G, Blanc M, Aragno M (1998) Bacterial diversity in the bulk soil and rhizosphere fractions of Lolium perenne and Trifolium repens as revealed by PCR restriction analysis of 16S rDNA. Plant Soil 198:219–224CrossRefGoogle Scholar
  23. 23.
    Acosta-Martinez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770CrossRefGoogle Scholar
  24. 24.
    Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230PubMedCrossRefGoogle Scholar
  25. 25.
    Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13PubMedCrossRefGoogle Scholar
  26. 26.
    StreitwolfEngel R, Boller T, Wiemken A, Sanders IR (1997) Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. J Ecol 85:181–191CrossRefGoogle Scholar
  27. 27.
    Newsham KK, Fitter AH, Watkinson AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000CrossRefGoogle Scholar
  28. 28.
    Brundrett M (1991) Mycorrhizas in Natural Ecosystems. Adv Ecol Res 21:171–313CrossRefGoogle Scholar
  29. 29.
    Miethling R, Wieland G, Backhaus H, Tebbe CC (2000) Variation of microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microbial Ecol 40:43–56Google Scholar
  30. 30.
    McCaig AE, Glover LA, Prosser JI (1999) Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl Environ Microbiol 65:1721–1730PubMedGoogle Scholar
  31. 31.
    Nunan N, Daniell TJ, Singh BK, Papert A, McNicol JW, Prosser JI (2005) Links between plant and rhizoplane bacterial communities in grassland soils, characterized using molecular techniques. Appl Environ Microbiol 71:6784–6792PubMedCrossRefGoogle Scholar
  32. 32.
    Teixeira LCRS, Peixoto RS, Cury JC, Sul WJ, Pellizari VH, Tiedje J, Rosado AS (2010) Bacterial diversity in rhizosphere soil from Antarctic vascular plants of Admiralty Bay, maritime Antarctica. ISME J 4:989–1001PubMedCrossRefGoogle Scholar
  33. 33.
    Buyer JS, Roberts DP, Russek-Cohen E (1999) Microbial community structure and function in the spermosphere as affected by soil and seed type. Can J Microbiol 45:138–144CrossRefGoogle Scholar
  34. 34.
    Dalmastri C, Chiarini L, Cantale C, Bevivino A, Tabacchioni S (1999) Soil type and maize cultivar affect the genetic diversity of maize root-associated Burkholderia cepacia populations. Microbial Ecol 38:273–284CrossRefGoogle Scholar
  35. 35.
    Day JM, Neves MCP, Döbereiner J (1974) Nitrogenase activity on the roots of tropical forage grasses. Soil Biol Biochem 7:107–112CrossRefGoogle Scholar
  36. 36.
    Döbereiner J, Day JM, Dart PJ (1972) Nitrogenase activity in the rhizosphere of sugar cane and some other tropical grasses. Plant Soil 37:191–196CrossRefGoogle Scholar
  37. 37.
    Gomes NCM, Heuer H, Schonfeld J, Costa R, Mendonca-Hagler L, Smalla K (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232:167–180CrossRefGoogle Scholar
  38. 38.
    Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J (2009) Metagenomic pyrosequencing and microbial identification. Clin Chem 55:856–866PubMedCrossRefGoogle Scholar
  39. 39.
    Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B, Schlapbach R, von Mering C, Vorholt JA (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc Natl Acad Sci U S A 106:16428–16433PubMedCrossRefGoogle Scholar
  40. 40.
    Chun J, Kim KY, Lee JH, Choi Y (2010) The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX Titanium pyrosequencer. BMC Microbiol 10:101PubMedCrossRefGoogle Scholar
  41. 41.
    Unno T, Jang J, Han D, Kim JH, Sadowsky MJ, Kim OS, Chun J, Hur HG (2010) Use of barcoded pyrosequencing and shared OTUs to determine sources of fecal bacteria in watersheds. Environ Sci Technol 44:7777–7782PubMedCrossRefGoogle Scholar
  42. 42.
    Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721PubMedCrossRefGoogle Scholar
  43. 43.
    Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorials. Primer-E Ltd, PlymouthGoogle Scholar
  44. 44.
    White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Compute Biol 5:e1000352CrossRefGoogle Scholar
  45. 45.
    Suarez-Moreno ZR, Caballero-Mellado J, Coutinho BG, Mendonca-Previato L, James EK, Venturi V (2012) Common features of environmental and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266PubMedCrossRefGoogle Scholar
  46. 46.
    Caballero-Mellado J, Martinez-Aguilar L, Paredes-Valdez G, Santos PE (2004) Burkholderia unamae sp. nov., an N2-fixing rhizospheric and endophytic species. Int J Syst Evol Microbiol 54:1165–1172PubMedCrossRefGoogle Scholar
  47. 47.
    Reis VM, Estrada-de los Santos P, Tenorio-Salgado S, Vogel J, Stoffels M, Guyon S, Mavingui P, Baldani VL, Schmid M, Baldani JI, Balandreau J, Hartmann A, Caballero-Mellado J (2004) Burkholderia tropica sp. nov., a novel nitrogen-fixing, plant-associated bacterium. Int J Syst Evol Microbiol 54:2155–2162PubMedCrossRefGoogle Scholar
  48. 48.
    Chen WM, de Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JP, Vandamme P (2008) Burkholderia sabiae sp. nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58:2174–2179PubMedCrossRefGoogle Scholar
  49. 49.
    Caballero-Mellado J, Onofre-Lemus J, Estrada-de Los Santos P, Martinez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319PubMedCrossRefGoogle Scholar
  50. 50.
    Kim M, Singh D, Lai-Hoe A, Go R, Abdul Rahim R, NA A, Chun J, Adams JM (2012) Distinctive phyllosphere bacterial communities in tropical trees. Microb Ecol 63:674–681PubMedCrossRefGoogle Scholar
  51. 51.
    Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant–microbe–soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291CrossRefGoogle Scholar
  52. 52.
    Singh BK, Nunan N, Ridgway KP, McNicol J, Young JPW, Daniell TJ, Prosser JI, Millard P (2008) Relationship between assemblages of mycorrhizal fungi and bacteria on grass roots. Environ Microbiol 10:534–541PubMedCrossRefGoogle Scholar
  53. 53.
    Wamberg C, Christensen S, Jakobsen I, Muller AK, Sorensen SJ (2003) The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol Biochem 35:1349–1357CrossRefGoogle Scholar
  54. 54.
    Olsson PA, Wallander H (1998) Interactions between ectomycorrhizal fungi and the bacterial community in soils amended with various primary minerals. FEMS Microbiol Ecol 27:195–205CrossRefGoogle Scholar
  55. 55.
    de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811PubMedCrossRefGoogle Scholar
  56. 56.
    Dixona RK, Gargb VK, Raoc MV (1993) Inoculation of Leucaena and Prosopis seedlings with Glomus and Rhizobium species in saline soil: rhizosphere relations and seedling growth. Arid Soil Res Rehabil 7:133–144Google Scholar
  57. 57.
    Mangan SA, Schnitzer SA, Herre EA, Mack KM, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755PubMedCrossRefGoogle Scholar
  58. 58.
    Timonen S, Hurek T (2006) Characterization of culturable bacterial populations associating with Pinus sylvestrisSuillus bovinus mycorrhizospheres. Can J Microbiol 52:769–778PubMedCrossRefGoogle Scholar
  59. 59.
    Kielak A, Pijl AS, van Veen JA, Kowalchuk GA (2008) Differences in vegetation composition and plant species identity lead to only minor changes in soil-borne microbial communities in a former arable field. FEMS Microbiol Ecol 63:372–382PubMedCrossRefGoogle Scholar
  60. 60.
    Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, Estrada-de los Santos P, Gross E, DosReis FB, Sprent JI, Young JPW, James EK (2011) Legume-nodulating Betaproteobacteria: diversity, host range, and future prospects. Mol Plant Microbe In 24:1276–1288CrossRefGoogle Scholar
  61. 61.
    Pagan JD, Child JJ, Scowcroft WR, Gibson AH (1975) Nitrogen-fixation by Rhizobium cultured on a defined medium. Nature 256:406–407CrossRefGoogle Scholar
  62. 62.
    Kim M, Singh D, Lai-Hoe A, Go R, Abdul Rahim R, A NA, Chun J, Adams JM (2011) Distinctive phyllosphere bacterial communities in tropical trees. Microb EcolGoogle Scholar
  63. 63.
    Chiu CH, Waddingdon M, Hsieh WS, Greenberg D, Schreckenberger PC, Carnahan AM (2000) Atypical Chryseobacterium meningosepticum and meningitis and sepsis in newborns and the immunocompromised, Taiwan. Emerg Infect Dis 6:481–486PubMedCrossRefGoogle Scholar
  64. 64.
    Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364PubMedCrossRefGoogle Scholar
  65. 65.
    Yergeau E, Kang S, He Z, Zhou J, Kowalchuk GA (2007) Functional microarray analysis of nitrogen and carbon cycling genes across an Antarctic latitudinal transect. ISME J 1:163–179PubMedCrossRefGoogle Scholar
  66. 66.
    Brejda JJ, Moser LE, Vogel KP (1998) Evaluation of switchgrass rhizosphere microflora for enhancing seedling yield and nutrient uptake. Agron J 90:753–758CrossRefGoogle Scholar
  67. 67.
    Edwards DP, Fisher B, Boyd E (2010) Protecting degraded rainforests: enhancement of forest carbon stocks under REDD. Conserv Lett 3:313–316CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Yoon Myung Oh
    • 1
  • Mincheol Kim
    • 1
  • Larisa Lee-Cruz
    • 1
  • Ang Lai-Hoe
    • 2
  • Rusea Go
    • 3
  • N. Ainuddin
    • 4
  • Raha Abdul Rahim
    • 5
  • Noraini Shukor
    • 4
  • Jonathan M. Adams
    • 1
  1. 1.School of Biological SciencesSeoul National UniversityGwanak-guRepublic of Korea
  2. 2.Division of Forest BiotechnologyForest Research Institute of MalaysiaKepongMalaysia
  3. 3.Department of BiologyUniversiti Putra MalaysiaSerdangMalaysia
  4. 4.INTROPUniversiti Putra MalaysiaSerdangMalaysia
  5. 5.Faculty of Biotechnology and Biomolecular Science, Institute of BioscienceUniversiti Putra MalaysiaSerdangMalaysia

Personalised recommendations