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Biology and Fertility of Soils

, Volume 48, Issue 6, pp 651–663 | Cite as

Biochemical characterization with detection and expression of bacterial β-glucosidase encoding genes of a Mediterranean soil under different long-term management practices

  • Rosa Cañizares
  • Beatriz Moreno
  • Emilio BenitezEmail author
Original Paper

Abstract

Mediterranean agroecosystems are particularly vulnerable to soil degradation, and alterations in ecosystem services need to be predicted using appropriate approaches. In the present work, we perform an integrated assessment of soils under different long-term management practices—tillage vs. covered soils—under semiarid conditions by using a complementary soil biochemical, genomic, and transcriptomic approach. Dehydrogenase, β-glucosidase, phosphatase, urease and arylsulphatase activities were determined, as well as both overall and metabolically active bacterial population number and community structure. In addition, this is the first report linking β-glucosidase activity with genes encoding bacterial β-glucosidases in soil, a key enzyme involved in soil–carbon cycle. In our work, data on bacterial biomass or β-glucosidase gene copy number has provided no additional information regarding the effect of management or profile depth on soil bacteria behaviour other than those derived from traditional biochemical methods measuring overall microbial activity potential. Nevertheless, a different trend resulted when gene transcripts were considered pointing to the relevance of using RNA-related properties as sensitive indicators of bacterial physiological state in semiarid soils. The results evidenced the influence of management and soil depth on the expression of bacterial β-glucosidase genes, which was by no means related to available C-nutrients. The results also pointed out overexpression of ribosomal RNA genes in tillage soils. This fact was not an indication of higher bacterial biomass but probably the response of the bacterial community to stressed conditions. Consequence of this would be the positive effect of spontaneous cover crops on soil biological stability, where bacterial metabolic expense was much lower.

Keywords

Agroecosystem functioning Genomics Semiarid climate Soil enzymes Transcriptomics Vulnerable ecosystems 

Notes

Acknowledgements

This work was supported by ERDF-co-financed grant CGL2009-07907 from the Spanish Ministry of Science of Innovation. R. Cañizares is supported by the JAE-CSIC predoctoral Program. We would like to thank David Nesbitt for the valuable English editing on the latest version of the manuscript. Finally, we would also like to thank Prof. P. Nannipieri and two anonymous reviewers for their helpful comments that greatly improved the manuscript.

Supplementary material

374_2012_663_MOESM1_ESM.doc (34 kb)
ESM 1 (DOC 34 kb)

References

  1. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944CrossRefGoogle Scholar
  2. Bandick AK, Dick RP (1999) Field management effects on soil enzyme activities. Soil Biol Biochem 31:1471–1479CrossRefGoogle Scholar
  3. Bending GD, Turner MK, Rayns F, Marx M-C, Wood M (2004) Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes. Soil Biol Biochem 36:1785–1792CrossRefGoogle Scholar
  4. Benitez E, Nogales R, Elvira C, Masciandaro G, Ceccanti B (1999) Enzyme activities as indicators of the stabilization of sewage sludges composting with Eisenia foetida. Bioresource Technol 67:297–303CrossRefGoogle Scholar
  5. Benitez E, Nogales R, Campos M, Ruano F (2006) Biochemical variability of olive-orchard soils under different management systems. Appl Soil Ecol 32:221–231CrossRefGoogle Scholar
  6. Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Global Chang Biol 15:808–824CrossRefGoogle Scholar
  7. Bremner JM (1978) Urease activity in soils. In: Burns RG (ed) Soil enzymes. Academic, London, pp 149–197Google Scholar
  8. Burns RG (1978) Enzyme activity in soil: some theoretical and practical considerations. In: Burns RG (ed) Soil enzymes. Academic, London, pp 295–339Google Scholar
  9. Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427CrossRefGoogle Scholar
  10. Cañizares R, Benitez E, Ogunseitan OA (2011) Molecular analyses of [beta]-glucosidase diversity and function in soil. Eur J Soil Biol 47:1–8CrossRefGoogle Scholar
  11. Castro J, Fernández-Ondoño E, Rodríguez C, Lallena AM, Sierra M, Aguilar J (2008) Effects of different olive-grove management systems on the organic carbon and nitrogen content of the soil in Jaén (Spain). Soil Till Res 98:56–67CrossRefGoogle Scholar
  12. Cui W, Taub DD, Gardner K (2007) qPrimerDepot: a primer database for quantitative real time PCR. Nucleic Acids Res 35:D805–D809PubMedCrossRefGoogle Scholar
  13. Di Gennaro P, Moreno B, Annoni E, García-Rodríguez S, Bestetti G, Benitez E (2009) Dynamic changes in bacterial community structure and in naphthalene dioxygenase expression in vermicompost-amended PAH-contaminated soils. J Hazar Mater 172:1464–1469CrossRefGoogle Scholar
  14. Duineveld BM, Kowalchuk GA, Keijzer A, Van Elsas JD, Van Veen JA (2001) Analysis of bacterial communities in the rhizosphere of chrysanthemum via denaturing gradient gel electrophoresis of PCR-amplified 16S rRNA as well as DNA fragments coding for 16S rRNA. Appl Environ Microbiol 67:172–178PubMedCrossRefGoogle Scholar
  15. European Council (2008) Agriculture Council Political Agreement on the Health Check. 20 November 2008, 16049/08Google Scholar
  16. FAO (1998) World reference base for soil resources. World Soil Resources Reports 84. FAO-ISRIC-ISSS, RomeGoogle Scholar
  17. Geisseler D, Horwath WR (2009) Short-term dynamics of soil carbon, microbial biomass, and soil enzyme activities as compared to longer-term effects of tillage in irrigated row crops. Biolo Fertil Soils 46:65–72CrossRefGoogle Scholar
  18. Gómez JA, Álvarez S, Soriano M-A (2009) Development of a soil degradation assessment tool for organic olive groves in southern Spain. Catena 79:9–17CrossRefGoogle Scholar
  19. Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2003) Physiological and community responses of established grassland bacterial populations to water stress. Appl Environ Microbiol 69:6961–6968PubMedCrossRefGoogle Scholar
  20. Hammer Ø, Harper DAT, Ryan PD (2001) Past: paleontological statistics software package for education and data analysis. Palaeontol Electr 4:1–9Google Scholar
  21. Hirsch PR, Mauchline TH, Clark IM (2010) Culture-independent molecular techniques for soil microbial ecology. Soil Biol Biochem 42:878–887CrossRefGoogle Scholar
  22. Hoshino YT, Matsumoto N (2007) DNA- versus RNA-based denaturing gradient gel electrophoresis profiles of a bacterial community during replenishment after soil fumigation. Soil Biol Biochem 39:434–444CrossRefGoogle Scholar
  23. Ibekwe AM, Grieve CM (2004) Changes in developing plant microbial community structure as affected by contaminated water. FEMS Microbiol Ecol 48:239–248PubMedCrossRefGoogle Scholar
  24. Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728PubMedCrossRefGoogle Scholar
  25. Jossi M, Fromin N, Tarnawski S, Kohler F, Gillet F, Aragno M, Hamelin J (2006) How elevated pCO2 modifies total and metabolically active bacterial communities in the rhizosphere of two perennial grasses grown under field conditions. FEMS Microbiol Ecol 55:339–350PubMedCrossRefGoogle Scholar
  26. Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66:1328–1333PubMedCrossRefGoogle Scholar
  27. Lal R (2011) Sequestering carbon in soils of agro-ecosystems. Food Policy 36:S33–S39CrossRefGoogle Scholar
  28. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[delta][delta]CT method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  29. MacQuillan AM, Halvorson HO (1962) Metabolic control of β-glucosidase synthesis in yeast. J Bacteriol 84:23–30PubMedGoogle Scholar
  30. Madejon E, Murillo JM, Moreno F, López MV, Arrue JL, Alvaro-Fuentes J, Cantero C (2009) Effect of long-term conservation tillage on soil biochemical properties in Mediterranean Spanish areas. Soil Till Res 105:55–62CrossRefGoogle Scholar
  31. 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
  32. Medina F, Iglesias A (2010) Agricultural practices with greenhouse mitigation potential in Mediterranean countries: evaluation and policy implications. Proceedings of the 9th European IFSA Symposium, ViennaGoogle Scholar
  33. Mijangos I, Garbisu C (2010) Consequences of soil sampling depth during the assessment of the effects of tillage and fertilization on soil quality: a common oversight. Soil Till Res 109:169–173CrossRefGoogle Scholar
  34. Monard C, Martin-Laurent F, Devers-Lamrani M, Lima O, Vandenkoornhuyse P, Binet F (2010) atz gene expressions during atrazine degradation in the soil drilosphere. Mol Ecol 19:749–759PubMedCrossRefGoogle Scholar
  35. Moreno B, Garcia-Rodriguez S, Cañizares R, Castro J, Benítez E (2009a) Rainfed olive farming in south-eastern Spain: long-term effect of soil management on biological indicators of soil quality. Agr Ecosys Environ 131:333–339CrossRefGoogle Scholar
  36. Moreno B, Vivas A, Nogales R, Macci C, Masciandaro G, Benitez E (2009b) Restoring biochemical activity and bacterial diversity in a trichloroethylene-contaminated soil: the reclamation effect of vermicomposted olive wastes. Environ Sci Poll Res 16:253–264CrossRefGoogle Scholar
  37. Muyzer G, De Waal EC, Uitterlinden AG (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 59:695–700PubMedGoogle Scholar
  38. Nannipieri P (2006) Role of stabilized enzymes in microbial ecology and enzyme extraction from soil with potential applications in soil proteomics. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil, vol 8. Springer, Berlin, pp 217–255CrossRefGoogle Scholar
  39. Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity ecology and applications. Marcel Dekker, New York, pp 1–33Google Scholar
  40. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  41. Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis: part 2. American Society of Agronomy, Madison, pp 539–578Google Scholar
  42. Newman T, de Bruijn FJ, Green P, Keegstra K, Kende H, McIntosh L, Ohlrogge J, Raikhel N, Somerville S, Thomashow M, Retzel E, Somerville C (1994) Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol 106:1241–1255PubMedCrossRefGoogle Scholar
  43. Niemi RM, Vepsäläinen M, Wallenius K, Simpanen S, Alakukku L, Pietola L (2005) Temporal and soil depth-related variation in soil enzyme activities and in root growth of red clover (Trifolium pratense) and timothy (Phleum pratense) in the field. Appl Soil Ecol 30:113–125CrossRefGoogle Scholar
  44. Norris TB, McDermott TR, Castenholz RW (2002) The long-term effects of UV exclusion on the microbial composition and photosynthetic competence of bacteria in hot-spring microbial mats. FEMS Microbiol Ecol 39:193–209PubMedCrossRefGoogle Scholar
  45. Novak JM, Bauer PJ, Hunt PG (2007) Carbon dynamics under long-term conservation and disk tillage management in a Norfolk loamy sand. Soil Sci Soc Am J 7:453–456CrossRefGoogle Scholar
  46. Odum EP (1985) Trends expected in stressed ecosystems. BioScience 35:419–422CrossRefGoogle Scholar
  47. Ogunseitan OA (2006) Soil proteomics: extraction and analysis of proteins from soil. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil, vol 8. Springer, Berlin, pp 95–115CrossRefGoogle Scholar
  48. Post WM, Know KC (2000) Soil carbon sequestration and land-use change: processes and potential. Glob Change Biol 6:317–327CrossRefGoogle Scholar
  49. Qian H, Hu B, Cao D, Chen W, Xu X, Lu Y (2007) Bio-safety assessment of validamycin formulation on bacterial and fungal biomass in soil monitored by real-time PCR. B Environ Cont Toxicol 78:239–244CrossRefGoogle Scholar
  50. Raup DM, Crick RE (1979) Measurement of faunal similarity in paleontology. J Paleontol 53:1213–1227Google Scholar
  51. Reeve JR, Schadt CW, Carpenter-Boggs L, Kang S, Zhou J, Reganold JP (2010) Effects of soil type and farm management on soil ecological functional genes and microbial activities. ISME J 4:1099–1107PubMedCrossRefGoogle Scholar
  52. Richards LA (1941) A pressure-membrane extraction apparatus for soil solution. Soil Sci 51:377–386CrossRefGoogle Scholar
  53. Rowan AK, Snape JR, Fearnside D, Barer MR, Curtis TP, Head IM (2003) Composition and diversity of ammonia-oxidising bacterial communities in wastewater treatment reactors of different design treating identical wastewater. FEMS Microbiol Ecol 43:195–206PubMedCrossRefGoogle Scholar
  54. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394PubMedCrossRefGoogle Scholar
  55. Schwieger F, Tebbe CC (1998) A new approach to utilize PCR-single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis. Appl Environ Microbiol 64:4870–4876PubMedGoogle Scholar
  56. Six J, Elliott ET, Paustian K (1999) Aggregate and soil organic matter dynamics under conventional and No-tillage systems. Soil Sci Soc Am J 63:1350–1358CrossRefGoogle Scholar
  57. Six J, Paustian K, Elliott ET, Combrink C (2000) Soil structure and organic matter. Soil Sci Soc Am J 64:681–689CrossRefGoogle Scholar
  58. Smith CJ, Nedwell DB, Dong LF, Osborn AM (2006) Evaluation of quantitative polymerase chain reaction-based approaches for determining gene copy and gene transcript numbers in environmental samples. Environ Microbiol 8:804–815PubMedCrossRefGoogle Scholar
  59. Sofo A, Palese AM, Casacchia T, Celano G, Ricciuti P, Curci M, Crecchio C, Xiloyannis C (2010) Genetic, functional, and metabolic responses of soil microbiota in a sustainable olive orchard. Soil Sci 175:81–88CrossRefGoogle Scholar
  60. Speir TW, Ross DJ (1978) Soil phosphatase and sulphatase. In: Burns RG (ed) Soil enzymes. Academic, London, pp 198–250Google Scholar
  61. Stromberger ME, Shah Z, Westfall DG (2011) High specific activity in low microbial biomass soils across a no-till evapotranspiration gradient in Colorado. Soil Biol Biochem 43:97–105CrossRefGoogle Scholar
  62. Vivas A, Moreno B, Garcia-Rodriguez S, Benitez E (2009) Assessing the impact of composting and vermicomposting on bacterial community size and structure, and microbial functional diversity of an olive-mill waste. Biores Technol 100:1319–1326CrossRefGoogle Scholar
  63. Wallis PD, Haynes RJ, Hunter CH, Morris CD (2010) Effect of land use and management on soil bacterial biodiversity as measured by PCR-DGGE. Appl Soil Ecol 46:147–150CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Rosa Cañizares
    • 1
  • Beatriz Moreno
    • 1
  • Emilio Benitez
    • 1
    Email author
  1. 1.Department of Environmental ProtectionEstación Experimental del Zaidín (EEZ), CSICGranadaSpain

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