Microbial Ecology

, Volume 69, Issue 4, pp 855–866 | Cite as

Amazonian Dark Earth and Plant Species from the Amazon Region Contribute to Shape Rhizosphere Bacterial Communities

  • Amanda Barbosa Lima
  • Fabiana Souza Cannavan
  • Acacio Aparecido Navarrete
  • Wenceslau Geraldes Teixeira
  • Eiko Eurya Kuramae
  • Siu Mui Tsai
Soil Microbiology


Amazonian Dark Earths (ADE) or Terra Preta de Índio formed in the past by pre-Columbian populations are highly sustained fertile soils supported by microbial communities that differ from those extant in adjacent soils. These soils are found in the Amazon region and are considered as a model soil when compared to the surrounding and background soils. The aim of this study was to assess the effects of ADE and its surrounding soil on the rhizosphere bacterial communities of two leguminous plant species that frequently occur in the Amazon region in forest sites (Mimosa debilis) and open areas (Senna alata). Bacterial community structure was evaluated using terminal restriction fragment length polymorphism (T-RFLP) and bacterial community composition by V4 16S rRNA gene region pyrosequencing. T-RFLP analysis showed effect of soil types and plant species on rhizosphere bacterial community structure. Differential abundance of bacterial phyla, such as Acidobacteria, Actinobacteria, Verrucomicrobia, and Firmicutes, revealed that soil type contributes to shape the bacterial communities. Furthermore, bacterial phyla such as Firmicutes and Nitrospira were mostly influenced by plant species. Plant roots influenced several soil chemical properties, especially when plants were grown in ADE. These results showed that differences observed in rhizosphere bacterial community structure and composition can be influenced by plant species and soil fertility due to variation in soil attributes.


Bacterial Community Soil Organic Carbon Rhizosphere Soil Control Soil Bacteroidetes 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank A.C.G. Souza, A.K. Silveira, M. Rüter, R.S. Macedo, and T.T. Souza for assistance with the fieldwork. We also thank Dr. L.A.G. de Souza (INPA) for providing seeds and helpful discussion. Thanks to M.G. Dumont for careful proofreading and comments. The authors acknowledge the financial support of CNPq—Conselho Nacional de Desenvolvimento Científico e Tecnológico and FAPESP—Fundação de Amparo à Pesquisa do Estado de São Paulo (2011/50914-3; 2011/51749-6). This research was supported by Embrapa Amazônia Ocidental and by FAPEAM—Fundação de Amparo à Pesquisa do Estado do Amazonas doctoral scholarship to the first author. Thanks are also given to the anonymous reviewers for their constructive comments. Publication 5619 Netherlands Institute of Ecology (NIOO-KNAW).


  1. 1.
    Jordan CF (1985) Nutrient cycling in tropical forest ecosystems: principles and their application in management and conservation. Wiley, New York, p 190Google Scholar
  2. 2.
    Costa ML, Kern DC (1999) Geochemical signatures of tropical soils with archaeological black earth in the Amazon. J Geochem Explor 66:369–385CrossRefGoogle Scholar
  3. 3.
    Grossman JM, O’Neill BE, Tsai SM, Liang B, Neves E, Lehmann J, Thies JE (2010) Amazonian Anthrosols support similar microbial communities that differ distinctly from those extant in adjacent, unmodified soils of the same mineralogy. Microb Ecol 60:192–205CrossRefPubMedGoogle Scholar
  4. 4.
    Navarrete AA, Cannavan FS, Taketani RG, Tsai SM (2010) A molecular survey of the diversity of microbial communities in different Amazonian agricultural model systems. Diversity 2:787–809CrossRefGoogle Scholar
  5. 5.
    O’Neill B, Grossman J, Tsai SM, Gomes JE, Lehmann J, Peterson J et al (2009) Bacterial community composition in Brazilian Anthrosol and adjacent soils characterized using culturing and molecular identification. Microb Ecol 58:23–35CrossRefPubMedGoogle Scholar
  6. 6.
    Taketani RG, Lima AB, Jesus EC, Teixeira WG, Tiedje JM, Tsai SM (2013) Bacterial community composition of anthropogenic biochar and Amazonian Anthrosols assessed by 16S rRNA gene 454 pyrosequencing. A van Leeuw J Microbiol 104:233–242CrossRefGoogle Scholar
  7. 7.
    Zhang FS (1993) Mobilization of iron and manganese by plant-borne and synthetic metal chelators. Plant Soil 155:111–114CrossRefGoogle Scholar
  8. 8.
    Haichar FE, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J et al (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230CrossRefPubMedGoogle Scholar
  9. 9.
    Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257CrossRefGoogle Scholar
  10. 10.
    Navarrete AA, Kuramae EE, de Hollander M, Pijl AS, van Veen JA, Tsai SM (2013) Acidobacterial community responses to agricultural management of soybean in Amazon forest soils. FEMS Microbiol Ecol 83:607–621CrossRefPubMedGoogle Scholar
  11. 11.
    Duineveld BM, Rosado AS, van Elsas JD, van Veen JA (1998) Analysis of the dynamics of bacterial communities in the rhizosphere of the chrysanthemum via denaturing gradient gel electrophoresis and substrate utilization patterns. Appl Environ Microbiol 64:4950–4957PubMedCentralPubMedGoogle Scholar
  12. 12.
    Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S et al (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751CrossRefPubMedCentralPubMedGoogle Scholar
  13. 13.
    Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Anton Leeuw Int J G 81:509–520CrossRefGoogle Scholar
  14. 14.
    Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM et al (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100CrossRefPubMedGoogle Scholar
  15. 15.
    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 69:1800–1809CrossRefPubMedCentralPubMedGoogle Scholar
  16. 16.
    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 71:6784–6792CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Alvey S, Yang CH, Buerkert A, Crowley DE (2003) Cereal/legume rotation effects on rhizosphere bacterial community structure in West African soils. Biol Fertil Soils 37:73–82Google Scholar
  18. 18.
    Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis—model and research methods. Soil Biol Biochem 43:883–894CrossRefGoogle Scholar
  19. 19.
    FAO (1988) World reference base for soil resources. World Soil Resources Report 84 FAO, Rome: 88.Google Scholar
  20. 20.
    Embrapa (1998) Análises químicas para avaliação da fertilidade do solo. Rio de Janeiro: Embrapa, CNPSo.Google Scholar
  21. 21.
    Lane, DJ (1991) 16S/23S rRNA sequencing. In: E. Stackebrandt, M. Goodfellow. Nucleic acid techniques in bacterial systematics. Wiley, New York, pp. 115–175.Google Scholar
  22. 22.
    Abdo Z, Schuette UME, Bent SJ, Williams CJ, Forney LJ, Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938CrossRefPubMedGoogle Scholar
  23. 23.
    Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinforma 10Google Scholar
  24. 24.
    Clarke, KR., Gorley, RN (2006) PRIMER v6: User Manual/Tutorial. Plymouth, UK: PRIMER-E.Google Scholar
  25. 25.
    Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  26. 26.
    Anderson, MJ., Gorley, RN., Clarke, KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth, UKGoogle Scholar
  27. 27.
    Marschner P, Grierson PF, Rengel Z (2005) Microbial community composition and functioning in the rhizosphere of three Banksia species in native woodland in Western Australia. Appl Soil Ecol 28:191–201CrossRefGoogle Scholar
  28. 28.
    Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415CrossRefGoogle Scholar
  29. 29.
    Goecks J, Nekrutenko A, Taylor J, Galaxy T (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11Google Scholar
  30. 30.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Reeder J, Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7:668–669CrossRefPubMedCentralPubMedGoogle Scholar
  32. 32.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedCentralPubMedGoogle Scholar
  33. 33.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  34. 34.
    Marschner H, Romheld V, Horst WJ, Martin P (1986) Root-induced changes in the rhizosphere—importance for the mineral-nutrition of plants. Z Pflanzenernähr Bodenkd 149:441–456CrossRefGoogle Scholar
  35. 35.
    Kuchenbuch R, Jungk A (1982) A method for determine concentration profiles at the soil–root interface by thin slicing rhizospheric soil. Plant Soil 68:391–394CrossRefGoogle Scholar
  36. 36.
    Hinsinger P, Gilkes RJ (1996) Mobilization of phosphate from phosphate rock and alumina-sorbed phosphate by the roots of ryegrass and clover as related to rhizosphere pH. Eur J Soil Sci 47:533–544CrossRefGoogle Scholar
  37. 37.
    Dinkelaker B, Romheld V, Marschner H (1989) Citric-acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292CrossRefGoogle Scholar
  38. 38.
    Norvell WA, Welch RM, Adams ML, Kochain LV (1993) Reduction of Fe(III), Mn(III), and Cu(II) chelates by roots of pea (Pisum sativum L) or soybean (Glycine max). Plant Soil 155:123–126CrossRefGoogle Scholar
  39. 39.
    Bambara S, Ndakidemi PA (2010) Changes in selected soil chemical properties in the rhizosphere of Phaseolus vulgaris L. supplied with Rhizobium inoculants, molybdenum and lime. Sci Res Essays 5:679–684Google Scholar
  40. 40.
    Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47CrossRefGoogle Scholar
  41. 41.
    Motavalli PP, Palm CA, Parton WJ, Elliott ET, Frey SD (1995) Soil pH and organic C dynamics in tropical forest soils: evidence from laboratory and simulation studies. Soil Biol Biochem 27:1589–1599CrossRefGoogle Scholar
  42. 42.
    Lehmann J, da Silva JP, Steiner C, Nehls T, Zech W, Glaser B (2003) Nutrient availability and leaching in an archaeological Anthrosol and a Ferralsol of the Central Amazon basin: fertilizer, manure and charcoal amendments. Plant Soil 249:343–357CrossRefGoogle Scholar
  43. 43.
    Bacilio-Jiménez M, Aguilar-Flores S, Ventura-Zapata E, Pérez-Campos E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249:271–277CrossRefGoogle Scholar
  44. 44.
    Kozdrój J, van Elsas JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32:1405–1417CrossRefGoogle Scholar
  45. 45.
    Jesus ED, Marsh TL, Tiedje JM, Moreira FMD (2009) Changes in land use alter the structure of bacterial communities in Western Amazon soils. ISME J 3:1004–1011CrossRefGoogle Scholar
  46. 46.
    Kuramae E, Gamper H, van Veen J, Kowalchuk G (2011) Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiol Ecol 77:285–294CrossRefPubMedGoogle Scholar
  47. 47.
    Singh BK, Munro S, Potts JM, Millard P (2007) Influence of grass species and soil type on rhizosphere microbial community structure in grassland soils. Appl Soil Ecol 36:147–155CrossRefGoogle Scholar
  48. 48.
    Kowalchuk GA, Stienstra AW, Heilig GHJ, Stephen JR, Woldendorp JW (2000) Changes in the community structure of ammonia-oxidizing bacteria during secondary succession of calcareous grasslands. Environ Microbiol 2:99–110CrossRefPubMedGoogle Scholar
  49. 49.
    Shi SJ, Richardson AE, O’Callaghan M, DeAngelis KM, Jones EE, Stewart A et al (2011) Effects of selected root exudate components on soil bacterial communities. FEMS Microbiol Ecol 77:600–610CrossRefPubMedGoogle Scholar
  50. 50.
    Jesus ED, Susilawati E, Smith SL, Wang Q, Chai BL, Farris R et al (2010) Bacterial communities in the rhizosphere of biofuel crops grown on marginal lands as evaluated by 16S rRNA gene pyrosequences. Bioenerg Res 3:20–27CrossRefGoogle Scholar
  51. 51.
    Kolton M, Harel YM, Pasternak Z, Graber ER, Elad Y, Cytryn E (2011) Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Appl Environ Microbiol 77:4924–4930CrossRefPubMedCentralPubMedGoogle Scholar
  52. 52.
    Chaudhry V, Rehman A, Mishra A, Chauhan PS, Nautiyal CS (2012) Changes in bacterial community structure of agricultural land due to long-term organic and chemical amendments. Microb Ecol 64:450–460CrossRefPubMedGoogle Scholar
  53. 53.
    Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261:199–208CrossRefGoogle Scholar
  54. 54.
    Oh YM, Kim M, Lee-Cruz L, Lai-Hoe A, Go R, Ainuddin N, Rahim RA, Shukor N, Adams JM (2012) Distinctive bacterial communities in the rhizoplane of four tropical tree species. Microb Ecol 64:1018–1027CrossRefPubMedGoogle Scholar
  55. 55.
    Kim MK, Jung H-Y (2007) Chitinophaga terrae sp. nov., isolated from soil. Int J Syst Evol Microbiol 57:1721–1724CrossRefPubMedGoogle Scholar
  56. 56.
    DeAngelis KM, Brodie EL, DeSantis TZ, Andersen GL, Lindow SE, Firestone MK (2009) Selective progressive response of soil microbial community to wild oat roots. ISME J 3:168–178CrossRefPubMedGoogle Scholar
  57. 57.
    Acosta-Martinez V, Lascano R, Calderon F, Booker JD, Zobeck TM, Upchurch DR (2011) Dryland cropping systems influence the microbial biomass and enzyme activities in a semiarid sandy soil. Biol Fertil Soils 47:655–667CrossRefGoogle Scholar
  58. 58.
    Sanguin H, Remenant B, Dechesne A, Thioulouse J, Vogel TM, Nesme X et al (2006) Potential of a 16S rRNA-based taxonomic microarray for analyzing the rhizosphere effects of maize on Agrobacterium spp. and bacterial communities. Appl Environ Microbiol 72:4302–4312CrossRefPubMedCentralPubMedGoogle Scholar
  59. 59.
    Derakshani M, Lukow T, Liesack W (2001) Novel bacterial lineages at the (sub) division level as detected by signature nucleotide-targeted recovery of 16S rRNA genes from bulk soil and rice roots of flooded rice microcosms. Appl Environ Microbiol 67:623–631CrossRefPubMedCentralPubMedGoogle Scholar
  60. 60.
    Cleveland CC, Nemergut DR, Schmidt SK, Townsend AR (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry 82:229–240CrossRefGoogle Scholar
  61. 61.
    Postma J, Nijhuis EH, Someus E (2010) Selection of phosphorus solubilizing bacteria with biocontrol potential for growth in phosphorus rich animal bone charcoal. Appl Soil Ecol 46:464–469CrossRefGoogle Scholar
  62. 62.
    Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of micro-organisms: potentials and future trends. Appl Microbiol Biotechnol 71:137–144CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Amanda Barbosa Lima
    • 1
    • 4
  • Fabiana Souza Cannavan
    • 1
  • Acacio Aparecido Navarrete
    • 1
  • Wenceslau Geraldes Teixeira
    • 2
  • Eiko Eurya Kuramae
    • 3
  • Siu Mui Tsai
    • 1
  1. 1.Laboratory of Cellular and Molecular Biology, Center for Nuclear Energy in AgricultureUniversity of São PauloPiracicabaBrazil
  2. 2.Brazilian Agricultural Research Corporation-EMBRAPA SoilsRio de JaneiroBrazil
  3. 3.Department of Microbial EcologyNetherlands Institute of Ecology (NIOO-KNAW)WageningenThe Netherlands
  4. 4.Max Planck Institute for Terrestrial MicrobiologyMarburgGermany

Personalised recommendations