Advertisement

Biology and Fertility of Soils

, Volume 49, Issue 6, pp 735–745 | Cite as

Genetic diversity of bacterial β-glucosidase-encoding genes as a function of soil management

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

Abstract

This study is the first approach to evaluate the diversity of bacterial β-glucosidase-encoding gene sequences, aiming to identify the main environmental factors structuring bacterial β-glucosidase genetic diversity in semiarid soils. Two agricultural management systems, soils under spontaneous cover vegetation vs. noncovered herbicide-treated soils, were tested. The weed biomass generated in the former was estimated around 2,600 kg ha−1 year−1, whereas leaves and root exudates from olive trees were the only input of C biomass in the latter. Dendrograms generated from polymerase chain reaction–denaturing gradient gel electrophoresis profiles of bacterial β-glucosidase-encoding genes revealed two clusters determined by soil treatment and sharing <20 % similarity. The sequences of a total of 59 DNA fragments, representing 39 operational taxonomic units, were successfully determined. The Proteobacteria phylum clearly dominated all the soil samples, but representatives of Chloroflexi, Deinococci, Actinobacteria, Thermotogae, and Firmicutes class were also detected. Management strategies favoring the presence of spontaneous vegetation determined a higher genetic diversity of β-glucosidase-encoding genes of soil bacteria. However, since there is little information of β-glucosidase gene sequences available in databases, it is difficult to establish particular relationships between bacterial networks for C degradation and land use. Results from canonical correspondence analysis indicated that bacterial metabolic networks for oligomeric C substrates utilization were affected by the physicochemical properties of the soil; the uppermost 10 cm of covered soil clustered together and were positively correlated with some chemical properties related to soil fertility, whereas less influence of soil texture was observed for the deeper layers of bare soils.

Keywords

β-Glucosidase Cover crops Gene expression Genetic diversity Soil functions 

Notes

Acknowledgments

This work was supported by ERDF-cofinanced grant CGL2009-07907 from the Spanish Ministry of Science of Innovation. R. Cañizares is supported by the JAE-CSIC predoctoral program. We also thank J. Castro for providing some chemical and physical data for the soils used in this study and the anonymous reviewers comments that greatly improved the manuscript. The chromatographic analyses were made at the Scientific Instrumentation Service, Estación Experimental del Zaidín, CSIC, Granada, Spain.

References

  1. Allen DE, Singh BP, Dalal RC (2011) Soil health indicators under climate change: a review of current knowledge. In: Singh BP, Cowie AL, Chan KY (eds) Soil biology. Soil health and climate change. Springer, Berlin, pp 25–45CrossRefGoogle Scholar
  2. Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235PubMedCrossRefGoogle Scholar
  3. 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
  4. Busto MD, Ortega N, Perez-Mateos M (1995) Induction of β-glucosidase in fungal and soil bacterial cultures. Soil Biol Biochem 27:949–954CrossRefGoogle Scholar
  5. 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
  6. Cañizares R, Moreno B, Benitez E (2012a) Biochemical characterization with detection and expression of bacterial β-glucosidase encoding genes of a Mediterranean soil under different long-term management practices. Biol Fertil Soils 48:651–663CrossRefGoogle Scholar
  7. Cañizares R, Moreno B, Benitez E (2012b) Bacterial β-glucosidase function and metabolic activity depend on soil management in semiarid rainfed agriculture. Ecol Evol 2:727–731PubMedCrossRefGoogle Scholar
  8. Cardelli R, Marchini F, Saviozzi A (2012) Soil organic matter characteristics, biochemical activity and antioxidant capacity in Mediterranean land use systems. Soil Till Res 120:8–14CrossRefGoogle Scholar
  9. 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
  10. Degens BP, Schippers LA, Sparling GP, Vojvodic-Vokovic M (2000) Decreases in organic C reserves in soils can reduce the catabolic diversity of soil microbial communities. Soil Biol Biochem 32:189–196CrossRefGoogle Scholar
  11. Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606CrossRefGoogle Scholar
  12. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50Google Scholar
  13. FAO (1998) World reference base for soil resources. World Soil Resources Reports 84, FAO-ISRIC-ISSS, RomeGoogle Scholar
  14. Fernandez I, Mahieu N, Cadisch G (2003) Carbon isotopic fractionation during decomposition of plant materials of different quality. Global Biogeochem Cy 17:1075CrossRefGoogle Scholar
  15. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:1–9Google Scholar
  16. Klose SK, Tabatabai MT (2002) Response of glycosidases in soils to chloroform fumigation. Biol Fertil Soils 35:262–269CrossRefGoogle Scholar
  17. Knight TR, Dick RP (2004) Differentiating microbial and stabilized β-glucosidase activity relative to soil quality. Soil Biol Biochem 36:2089–2096CrossRefGoogle Scholar
  18. Li YN, Porter AW, Mumford A, Zhao XH, Young LY (2012) Bacterial community structure and bamA gene diversity in anaerobic degradation of toluene and benzoate under denitrifying conditions. J Appl Microbiol 112:269–27PubMedCrossRefGoogle Scholar
  19. Mao Y, Yannarell AC, Mackie RI (2011) Changes in N-transforming archaea and bacteria in soil during the establishment of bioenergy crops. PLoS One 6:e24750. doi: 10.1371/journal.pone.0024750 PubMedCrossRefGoogle Scholar
  20. Matsumoto K, Kawamura K, Uchida M, Shibata Y (2007) Radiocarbon content and stable carbon isotopic ratios of individual fatty acids in subsurface soil: implication for selective microbial degradation and modification of soil organic matter. Geochem J 41:483–492CrossRefGoogle Scholar
  21. Metzger MJ, Rounsevell MDA, Acosta-Michlik L, Leemans R, Schröter D (2006) The vulnerability of ecosystem services to land use change. Agr Ecosyst Environ 114:69–85CrossRefGoogle Scholar
  22. Moscatelli MC, Lagomarsino A, Garzillo AMV, Pignataro A, Grego S (2012) β-Glucosidase kinetic parameters as indicators of soil quality under conventional and organic cropping systems applying two analytical approaches. Ecol Ind 13:322–327CrossRefGoogle Scholar
  23. 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 Microb 59:695–700Google Scholar
  24. Naafs DFW, Van Bergen PF, Boogert SJ, De Leeuw JW (2004) Solvent-extractable lipids in an acid andic forest soil; variations with depth and season. Soil Biol Biochem 36:297–308CrossRefGoogle Scholar
  25. 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
  26. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. P Natl Acad Sci Usa 76:5269–5273CrossRefGoogle Scholar
  27. 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
  28. 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
  29. Raup DM, Crick RE (1979) Measurement of faunal similarity in paleontology. J Paleontol 53:1213–1227Google Scholar
  30. Resat H, Bailey V, McCue LA, Konopka A (2012) Modeling microbial dynamics in heterogeneous environments: growth on soil carbon sources. Microb Ecol 63:883–897PubMedCrossRefGoogle Scholar
  31. 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
  32. Rubino M, Lubritto C, D’Onofrio A, Terrasi F, Kramer C, Gleixner G, Cotrufo M (2009) Isotopic evidences for microbiologically mediated and direct C input to soil compounds from three different leaf litters during their decomposition. Environ Chem Lett 7:85–95PubMedCrossRefGoogle Scholar
  33. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbio 75:7537–7541CrossRefGoogle Scholar
  34. 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
  35. Shackle VJ, Freeman C, Reynolds B (2000) Carbon supply and the regulation of enzyme activity in constructed wetlands. Soil Biol Biochem 32:1935–1940CrossRefGoogle Scholar
  36. Stevenson FJ, Cole MA (1999) Cycles of soil: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley, New York, 427 ppGoogle Scholar
  37. Stott DE, Andrews SS, Liebig MA, Wienhold BJ, Karlen DL (2010) Evaluation of β-glucosidase activity as a soil quality indicator for the soil management assessment framework. Soil Sci Soc Am J 74:107–119CrossRefGoogle Scholar
  38. Štursová M, Baldrian P (2011) Effects of soil properties and management on the activity of soil organic matter transforming enzymes and the quantification of soil-bound and free activity. Plant Soil 338:99–110CrossRefGoogle Scholar
  39. Ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, Available at http://www.canoco.comGoogle Scholar
  40. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  41. Trasar-Cepeda C, Gil-Sotres F, Leirós MC (2007) Thermodynamic parameters of enzymes in grassland soils from Galicia, NW Spain. Soil Biol Biochem 39:311–319CrossRefGoogle Scholar
  42. 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
  43. Zimmerman AR, Ahn MY (2011) Organo-mineral–enzyme interaction and soil enzyme activity. In: Shukla G, Varma A (eds) Soil enzymology. Springer, Berlin, pp 271–292Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

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

Personalised recommendations