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Antonie van Leeuwenhoek

, Volume 107, Issue 4, pp 935–949 | Cite as

Microbiological functioning, diversity, and structure of bacterial communities in ultramafic soils from a tropical savanna

  • Marco Pessoa-Filho
  • Cristine Chaves Barreto
  • Fábio Bueno dos Reis Junior
  • Rodrigo Rocha Fragoso
  • Flávio Silva Costa
  • Ieda de Carvalho Mendes
  • Leide Rovênia Miranda de Andrade
Original Paper

Abstract

Ultramafic soils are characterized by high levels of metals, and have been studied because of their geochemistry and its relation to their biological component. This study evaluated soil microbiological functioning (SMF), richness, diversity, and structure of bacterial communities from two ultramafic soils and from a non-ultramafic soil in the Brazilian Cerrado, a tropical savanna. SMF was represented according to simultaneous analysis of microbial biomass C (MBC) and activities of the enzymes β-glucosidase, acid phosphomonoesterase and arylsulfatase, linked to the C, P and S cycles. Bacterial community diversity and structure were studied by sequencing of 16S rRNA gene clone libraries. MBC and enzyme activities were not affected by high Ni contents. Changes in SMF were more related to the organic matter content of soils (SOM) than to their available Ni. Phylogeny-based methods detected qualitative and quantitative differences in pairwise comparisons of bacterial community structures of the three sites. However, no correlations between community structure differences and SOM or SMF were detected. We believe this work presents benchmark information on SMF, diversity, and structure of bacterial communities for a unique type of environment within the Cerrado biome.

Keywords

Cerrado Metals Soil enzymes Microbial biomass carbon 16S rRNA gene 

Notes

Acknowledgments

We thank Clodoaldo A. de Sousa, Lucas F.L.S. Rolim, Franciele Schlemmer, Leandro M. de Souza, and Milene R. Ribeiro, for their assistance during this study. We thank Fabiana de Gois Aquino for kindly providing images of the samples sites. We also thank Anglo American and their team at the Barro Alto plant for their support. This work was partially financed by, Embrapa Macroprograma 2—Grant# 02.07.01.007.00.00, Embrapa Macroprograma 3—Grant# 03.09.06.016.00.00, and the CNPq (National Council for Scientific and Technological Development) REPENSA call (562433/2010-4).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10482_2015_386_MOESM1_ESM.pdf (384 kb)
Online resource 1 (PDF 383 kb) Images of the two ultramafic sites selected for soil sampling. (A) Site 1, with a Campo Sujo physiognomy; (B) Site 2, with a Cerrado Ralo physiognomy. (Photo credit: Fabiana de Gois Aquino)
10482_2015_386_MOESM2_ESM.eps (3 mb)
Online resource 2 (EPS 3,059 kb) Neighbor-joining tree based on 16S rRNA gene sequences from Site 2 clones (in boldface) and their closest hits from RDP (with their corresponding accession numbers in parenthesis). Bootstrap values above 50 are shown. The tree was rooted with Methanocaldococcus jannaschii as an outgroup
10482_2015_386_MOESM3_ESM.eps (3 mb)
Online resource 3 (EPS 3,061 kb) Neighbor-joining tree based on 16S rRNA gene sequences from Cerrado clones (in boldface) and their closest hits from RDP (with their corresponding accession numbers in parenthesis). Bootstrap values above 50 are shown. The tree was rooted with Methanocaldococcus jannaschii as an outgroup
10482_2015_386_MOESM4_ESM.eps (3.8 mb)
Online resource 4 (EPS 3,929 kb) Rarefaction curves from Sites 1, 2 and Cerrado. Error bars represent the 95 % CI. Curves with different symbols represent clustering of sequences into OTUs identified by different dissimilarity cutoffs shown in the legend: unique (all unique sequences), 0.03 (3 % dissimilarity), 0.1 (10 % dissimilarity), 0.2 (20 % dissimilarity)

References

  1. Andrade LRM, Aquino FG, Miranda ZJG, Echevarria G, Becquer T, Nascimento CTC, Viana RM (2011) Assessment of Ni levels and plant species diversity in ultramafic soils under Ni mining in Barro Alto (GO)—Brazil. In: 7th international conference on serpentine ecology, 2011, Coimbra, Portugal, p 89Google Scholar
  2. Aquino FG, Viana RM, Miranda ZJG, Andrade LRM (2011a) Floristic composition in the ultramafic soils in Central Brazil. In: 7th international conference on serpentine ecology, 2011, Coimbra, Portugal, p 90Google Scholar
  3. Aquino FG, Viana RM, Miranda ZJG, Andrade LRM (2011b) Richness, abundance and species composition in different areas of the ultramafic soils in Central Brazil. In: 7th international conference on serpentine ecology, 2011, Coimbra, Portugal, p 91Google Scholar
  4. Araujo JF, de Castro AP, Costa MMC, Togawa RC, Júnior GJP, Quirino BF, Bustamante MMC, Williamson L, Handelsman J, Krüger RH (2012) Characterization of soil bacterial assemblies in Brazilian savanna-like vegetation reveals Acidobacteria dominance. Microb Ecol 64(3):760–770CrossRefPubMedGoogle Scholar
  5. Brookes PC, Mcgrath SP (1984) Effects of metal toxicity on the size of the soil microbial biomass. J Soil Sci 35:341–346CrossRefGoogle Scholar
  6. Brooks RR (1987) Serpentine and its vegetation: a multi-disciplinary approach. Dioscorides, Portland, ORGoogle Scholar
  7. Bunge J (2011) Estimating the number of species with CatchAll. Pac Symp Biocomput 11:121–130Google Scholar
  8. Chao A, Chazdon RL, Colwell RK, Shen T-J (2004) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159CrossRefGoogle Scholar
  9. Chou H, Holmes M (2001) DNA sequence quality trimming and vector removal. Bioinformatics 17:1093–1104CrossRefPubMedGoogle Scholar
  10. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37(database issue):D141–D145CrossRefPubMedCentralPubMedGoogle Scholar
  11. Daghino S, Murat C, Sizzano E, Girlanda M, Perotto S (2012) Fungal diversity is not determined by mineral and chemical differences in serpentine substrates. PLoS ONE 7:e44233CrossRefPubMedCentralPubMedGoogle Scholar
  12. Dawson JJC, Smith P (2007) Carbon losses from soil and its consequences for land-use management. Sci Total Environ 382:165–190CrossRefPubMedGoogle Scholar
  13. de Carvalho Mendes I, Fernandes MF, Chaer GM, dos Reis Junior FB (2012) Biological functioning of Brazilian Cerrado soils under different vegetation types. Plant Soil 359:183–195Google Scholar
  14. Doran JW, Zeiss MR (2000) Soil health and sustainability: managing the biotic component of soil quality. Appl Soil Ecol 15:3–11CrossRefGoogle Scholar
  15. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20Google Scholar
  16. Fliessbach A, Martens R, Reber HH (1994) Soil microbial biomass and microbial activity in soils treated with heavy-metal contaminated sewage-sludge. Soil Biol Biochem 26:1201–1205CrossRefGoogle Scholar
  17. Frostegard A, Tunlid A, Baath E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metals. Soil Biol Biochem 28:55–63CrossRefGoogle Scholar
  18. Gil-Sotres F, Trasar-Cepeda C, Leirós MC, Seoane S (2005) Different approaches to evaluating soil quality using biochemical properties. Soil Biol Biochem 37:877–887CrossRefGoogle Scholar
  19. Graffelman J (2013) calibrate: calibration of scatter plot and biplot axes. R package version 1.7.2. http://CRAN.R-project.org/package=calibrate
  20. Griffiths BS, DiazRavina M, Ritz K, McNicol JW, Ebblewhite N, Baath E (1997) Community DNA hybridisation and %G+C profiles of microbial communities from heavy metal polluted soils. FEMS Microbiol Ecol 24:103–112CrossRefGoogle Scholar
  21. Hattori H (1992) Influence of heavy metals on soil microbial activities. Soil Sci Plant Nutr 38:93–100CrossRefGoogle Scholar
  22. Herrera A, Hery M, Stach JEM, Jaffre T, Normand P, Navarro E (2007) Species richness and phylogenetic diversity comparisons of soil microbial communities affected by nickel-mining and revegetation efforts in New Caledonia. Eur J Soil Biol 43:130–139CrossRefGoogle Scholar
  23. Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677CrossRefPubMedCentralPubMedGoogle Scholar
  24. Jackson ML (1958) Soil chemical analysis. Prentice Hall, New YorkGoogle Scholar
  25. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453CrossRefPubMedCentralPubMedGoogle Scholar
  26. Kandeler E, Tscherko D, Bruce KD, Stemmer M, Hobbs PJ, Bardgett RD, Amelung W (2000) Structure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biol Fertil Soils 32:390–400CrossRefGoogle Scholar
  27. Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508PubMedGoogle Scholar
  28. Kozdrój J, van Elsas JD (2001) Structural diversity of microorganisms in chemically perturbed soil assessed by molecular and cytochemical approaches. J Microbiol Methods 43:197–212CrossRefPubMedGoogle Scholar
  29. Lane D (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  30. Lin C, Coleman NT (1965) The measurement of exchangeable aluminium in soil and clays. Soil Sci Soc Am Proc 29:374–378Google Scholar
  31. Lindsay WL, Norvell WA (1978) Development of a Dtpa soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428CrossRefGoogle Scholar
  32. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefPubMedCentralPubMedGoogle Scholar
  33. Lozupone CA, Hamady M, Kelley ST, Knight R (2007) Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Appl Environ Microbiol 73:1576–1585CrossRefPubMedCentralPubMedGoogle Scholar
  34. Ma Y, Rajkumar M, Freitas H (2009a) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75:719–725CrossRefPubMedGoogle Scholar
  35. Ma Y, Rajkumar M, Freitas H (2009b) Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. J Hazard Mater 166:1154–1161CrossRefPubMedGoogle Scholar
  36. McCune B, Mefford MJ (1999) Multivariate analysis of ecological data. MjM Software Design, Gleneden Beach, OregonGoogle Scholar
  37. Mengoni A, Barzanti R, Gonnelli C, Gabbrielli R, Bazzicalupo M (2001) Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ Microbiol 3:691–698CrossRefPubMedGoogle Scholar
  38. Mengoni A, Grassi E, Barzanti R, Biondi EG, Gonnelli C, Kim CK, Bazzicalupo M (2004) Genetic diversity of bacterial communities of serpentine soil and of rhizosphere of the nickel-hyperaccumulator plant Alyssum bertolonii. Microb Ecol 48(2):209–217Google Scholar
  39. Mirete S, de Figueras CG, González-Pastor JE (2007) Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Appl Environ Microbiol 73(19):6001–6011CrossRefPubMedCentralPubMedGoogle Scholar
  40. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762CrossRefGoogle Scholar
  41. Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. In: Sparks DL, Paga AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Summer ME (eds) Methods of soil analysis: chemical methods. Part 3. Soil Science Society of America, Madison, pp 961–1010Google Scholar
  42. Niklinska M, Chodak M, Laskowski R (2006) Pollution-induced community tolerance of microorganisms from forest soil organic layers polluted with Zn or Cu. Appl Soil Ecol 32:265–272CrossRefGoogle Scholar
  43. Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe J (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119:239–246CrossRefGoogle Scholar
  44. Oline DK (2006) Phylogenetic comparisons of bacterial communities from serpentine and nonserpentine soils. Appl Environ Microbiol 72:6965–6971CrossRefPubMedCentralPubMedGoogle Scholar
  45. Oliveira-Filho AT, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado Biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil—ecology and natural history of a neotropical savanna. Columbia University Press, New York, pp 91–120Google Scholar
  46. Peixoto RS, Chaer GM, Franco N, Reis Junior FB, Mendes IC, Rosado AS (2010) A decade of land use contributes to changes in the chemistry, biochemistry and bacterial community structures of soils in the Cerrado. Antonie Van Leeuwenhoek 98(3):403–413CrossRefPubMedGoogle Scholar
  47. Pennanen T (2001) Microbial communities in boreal coniferous forest humus exposed to heavy metals and changes in soil pH—a summary of the use of phospholipid fatty acids, Biolog (R) and H-3-thymidine incorporation methods in field studies. Geoderma 100:91–126CrossRefGoogle Scholar
  48. Prasad MNV, Freitas H, Fraenzle S, Wuenschmann S, Markert B (2010) Knowledge explosion in phytotechnologies for environmental solutions. Environ Pollut 158:18–23CrossRefPubMedGoogle Scholar
  49. Quirino BF, Pappas GJ, Tagliaferro AC, Collevatti RG, Neto EL, Da Silva MRSS, Bustamante MMC, Krüger RH (2009) Molecular phylogenetic diversity of bacteria associated with soil of the savanna-like Cerrado vegetation. Microbiol Res 164:59–70CrossRefPubMedGoogle Scholar
  50. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  51. Rajkumar M, Prasad MNV, Freitas H, Ae N (2009) Biotechnological applications of serpentine soil bacteria for phytoremediation of trace metals. Crit Rev Biotech 29:120–130CrossRefGoogle Scholar
  52. Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goias state, Brazil. Plant Soil 293:107–119CrossRefGoogle Scholar
  53. Renella G, Mench M, van der Lelie D, Pietramellara G, Ascher J, Ceccherini MT, Landi L, Nannipieri P (2004) Hydrolase activity, microbial biomass and community structure in long-term Cd-contaminated soils. Soil Biol Biochem 36:443–451CrossRefGoogle Scholar
  54. Renella G, Chaudri AM, Falloon CM, Landi L, Nannipieri P, Brookes PC (2007) Effects of Cd, Zn, or both on soil microbial biomass and activity in a clay loam soil. Biol Fertil Soils 43:751–758CrossRefGoogle Scholar
  55. Ribeiro JF, Walter BMT (1998) Fitofisionomias do bioma Cerrado. In: Sano SM, Almeida SP (eds) Cerrado: ambiente e flora. Embrapa-CPAC, Planaltina, Brazil, pp 87–166Google Scholar
  56. Sambrook JJ, Russel DDW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, New YorkGoogle Scholar
  57. Sandaa R, Torsvik V, Enger O, Daae FL, Castberg T, Hahn D (1999) Analysis of bacterial communities in heavy metal-contaminated soils at different levels of resolution. FEMS Microbiol Ecol 30:237–251CrossRefPubMedGoogle Scholar
  58. Schipper L, Lee W (2004) Microbial biomass, respiration and diversity in ultramafic soils of West Dome, New Zealand. Plant Soil 262:151–158CrossRefGoogle Scholar
  59. Schloss PD, Larget BR, Handelsman J (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70:5485–5492CrossRefPubMedCentralPubMedGoogle Scholar
  60. Schloss PD, Gevers D, Westcott SL (2011) Reducing the Effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS ONE 6:e27310CrossRefPubMedCentralPubMedGoogle Scholar
  61. Silva LJ (2010) laercio: Duncan test, Tukey test and Scott-Knott test. R package version 1.0-1. http://CRAN.R-project.org/package=laercio
  62. Sims JT (1989) Comparison of Mehlich 1 and Mehlich 3 extractants for P, K, Ca, Mg, Cu and Zn in Atlantic Coastal Plain Soils. Commun Soil Sci Plan 20:1707–1726CrossRefGoogle Scholar
  63. Soetaert K (2014) shape: functions for plotting graphical shapes, colors. R package version 1.4.1. http://CRAN.R-project.org/package=shape
  64. Stark CH, Condron LM, O’Callaghan M, Stewart A, Di HJ (2008) Differences in soil enzyme activities, microbial community structure and short-term nitrogen mineralisation resulting from farm management history and organic matter amendments. Soil Biol Biochem 40:1352–1363CrossRefGoogle Scholar
  65. Stefanowicz AM, Niklinska M, Laskowski R (2008) Metals affect soil bacterial and fungal diversity differently. Environ Toxicol Chem 27:591–598CrossRefPubMedGoogle Scholar
  66. Tabatabai MA (1970) Soil enzymes. In: Weaver RW, Angle S, Bottomley PJ et al (eds) Methods of soil analysis. Part 2: microbiological and biochemical properties. Soil Science Society of America, Madison, pp 775–833Google Scholar
  67. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedCentralPubMedGoogle Scholar
  68. Thomas GW (1982) Exchange cations. Method 9–3.1. In: Page AL (ed) Methods of soil analysis. Part 2. Chemical and Microbiological Properties, 2nd Ed., ASA, SSA, Madison, WI. pp 159–165Google Scholar
  69. Vance ED, Brookes PC, Jenkinson DS (1987) Microbial biomass measurements in forest soils—the use of the chloroform fumigation incubation method in strongly acid soils. Soil Biol Biochem 19:697–702CrossRefGoogle Scholar
  70. Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846CrossRefGoogle Scholar
  71. Wang Y, Shi J, Wang H, Lin Q, Chen X, Chen Y (2007) The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter. Ecotoxicol Environ Saf 67:75–81CrossRefPubMedGoogle Scholar
  72. Yao H, He Z, Wilson M, Campbell C (2000) Microbial biomass and community structure in a sequence of soils with increasing fertility and changing land use. Microb Ecol 40:223–237PubMedGoogle Scholar
  73. Zhou J, Xia B, Treves DS, Wu L-Y, Marsh TL, O’Neill RV, Palumbo AV, Tiedje JM (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68:326–334CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Marco Pessoa-Filho
    • 1
  • Cristine Chaves Barreto
    • 2
  • Fábio Bueno dos Reis Junior
    • 1
  • Rodrigo Rocha Fragoso
    • 1
  • Flávio Silva Costa
    • 2
  • Ieda de Carvalho Mendes
    • 1
  • Leide Rovênia Miranda de Andrade
    • 1
  1. 1.Embrapa CerradosBrasíliaBrazil
  2. 2.Graduate Program in Genomic Sciences and BiotechnologyUniversidade Católica de BrasíliaBrasíliaBrazil

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