Skip to main content
Log in

Biochemical properties and microbial community structure of five different soils after atrazine addition

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Atrazine is one of the most used herbicides worldwide; however, consequences of its long-term agricultural use are still unknown. A laboratory study was performed to examine changes in microbial properties following ethylamino-15N-atrazine addition, at recommended agronomic dose, to five acidic soils from Galicia (NW Spain) showing different physico-chemical characteristics, as well as atrazine application history. Net N mineralization was observed in all soils, with nitrate being the predominant substance formed. The highest values were detected in soils with low atrazine application history. From 2% to 23% of the atrazine-15N was found in the soil inorganic-N pool, the highest values being detected after 9 weeks in soils with longer atrazine application history and lower indigenous soil N mineralization. The application of atrazine slightly reduced the amount of soil N mineralized and microbial biomass at short term. Soluble carbohydrates and β-glucosidase and urease activity decreased with incubation time, but were not significantly affected by the single application of atrazine. Microbial community structure changed as consequence of both soil type and incubation time, but no changes in the phospholipid fatty acid (PLFA) pattern were detected due to recent atrazine addition at normal doses. The saturated 17- to 20-carbon fatty acids had higher relative abundance in soils with a longer atrazine history and fungal biomass, as indicated by the PLFA 18:2ω6,9, decreased with the incubation time. The results suggested that the PLFA pattern and soil N dynamics can detect the long-term impact of repeated atrazine application to agricultural soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abdelhafid R, Houot S, Barriuso E (2000a) Dependence of atrazine degradation on C and N availability in adapted and non-adapted soils. Soil Biol Biochem 32:389–401

    Article  CAS  Google Scholar 

  • Abdelhafid R, Houot S, Barriuso E (2000b) How increasing availabilities of carbon and nitrogen affect atrazine behaviour in soils. Biol Fertil Soils 30:333–340

    Article  CAS  Google Scholar 

  • Accinelli C, Giovanni D, Vicari A, Catizone P (2001) Atrazine and metolachlor degradation in subsoils. Biol Fertil Soils 33:495–500

    Article  CAS  Google Scholar 

  • Alvey S, Crowley DE (1995) Influence of organic amendments on biodegradation of atrazine as a nitrogen source. J Environ Qual 24:1156–1162

    Article  CAS  Google Scholar 

  • Assaf NA, Turco RF (1994) Influence of carbon and nitrogen application on the mineralization of atrazine and its metabolites in soil. Pest Sci 41:41–47

    Article  CAS  Google Scholar 

  • Bååth E, Nilsson LO, Göransson H, Wallander H (2004) Can the extent of degradation of soil fungal mycelium during soil incubation be use to estimate ectomycorrizal biomass in soil? Soil Biol Biochem 36:2105–2109

    Article  Google Scholar 

  • Barriuso E, Houot S (1996) Rapid mineralization of the s-triazine ring of atrazine in soils in relation to soil management. Soil Biol Biochem 28:1341–1348

    Article  CAS  Google Scholar 

  • Behki RM, Khan SU (1986) Degradation of atrazine by Pseudomonas: N-dealkylation and dehalogenation of atrazine and its metabolites. J Agr Food Chem 34:746–749

    Article  CAS  Google Scholar 

  • Bichat F, Sims GK, Mulvaney RL (1999) Microbial utilization of heterocyclic nitrogen from atrazine. Soil Sci Soc Am J 63:100–110

    Article  CAS  Google Scholar 

  • Bouquard C, Ouzzani J, Prome JC, Michael-Briand Y, Plesiat P (1997) Dechlorination of atrazine by a Rhizobium sp. isolate. Appl Environ Microbiol 63:862–866

    PubMed  CAS  Google Scholar 

  • Capriel P, Haisch A, Khan SU (1985) Distribution and nature of bound (nonextractable) residues of atrazine in a mineral soil nine years after herbicide application. J Agr Food Chem 33:567–569

    Article  CAS  Google Scholar 

  • Chang YJ, Hussain A, Stephen JR, Mullen MD, White DC, Peacock A (2001) Impact of herbicides on the abundance and structure of indigenous beta-subgroup ammonia-oxidizer communities in soil microcosms. Environ Toxicol Chem 20:2462–2468

    Article  Google Scholar 

  • Chen SK, Edwards CA, Subler S (2001) Effects of the fungicides benomyl, captan and chlorothalonil on soil microbial activity and nitrogen dynamics in laboratory incubations. Soil Biol Biochem 33:1971–1980

    Article  CAS  Google Scholar 

  • Cook AM (1987) Biodegradation of s-triazine xenobiotics. FEMS Microbiol Rev 46:93–116

    Article  CAS  Google Scholar 

  • Cook SM, Hütter R (1981) S-triazines as nitrogen sources for bacteria. J Agr Food Chem 29:1135–1143

    Article  CAS  Google Scholar 

  • Couto-Vázquez A, González-Prieto SJ (2006) Short- and medium-term effects of three fire fighting chemicals on the properties of a burnt soil. Sci Total Environ 371:353–361

    Article  PubMed  Google Scholar 

  • Davies H, Greaves MP (1981) Effects of some herbicides on soil enzyme activities. Weed Res 21:205–209

    Article  CAS  Google Scholar 

  • Dzantor EK, Felsot AS (1991) Microbial responses to large concentrations of herbicides in soil. Environ Toxicol Chem 10:649–655

    Article  CAS  Google Scholar 

  • Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606

    Article  CAS  Google Scholar 

  • Entry JA, Mattson KG, Emmingham WH (1993) The influence of N on atrazine and 2,4-dichlorophenoxyactetic acid mineralization in grassland soils. Biol Fertil Soils 16:179–182

    Article  CAS  Google Scholar 

  • Erickson LE, Lee KH (1989) Degradation of atrazine and related s-triazines. Crit Rev Environ Contr 19:1–14

    Article  CAS  Google Scholar 

  • Frostegård A, Bååth E (1996) The use of phospholipid fatty acid to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  • Frostegård A, Bååth E, Tunlid A (1993) Shifts in the structure of soil microbial communities in limed soils as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730

    Article  Google Scholar 

  • Frostegård A, Tunlid A, Bååth E (1996) Changes in microbial community structure during long-term incubation in two soils experimentally contaminated with metal. Soil Biol Biochem 28:55–63

    Article  Google Scholar 

  • Gan J, Becker RL, Koskinen WC, Buhler DD (1996) Degradation of atrazine in two soils as a function of concentration. J Environ Qual 25:1064–1072

    Article  CAS  Google Scholar 

  • Ghani A, Wardle DA, Rahman A, Lauren DR (1996) Interaction between 14C-labelled atrazine and the soil microbial biomass in relation to herbicide degradation. Biol Fertil Soils 21:17–22

    Article  CAS  Google Scholar 

  • Gianfreda L, Sannino F, Ortega N, Nannipieri P (1994) Activity of free and immobilized urease in soil: effects of pesticides. Soil Biol Biochem 26:77–784

    Article  Google Scholar 

  • Greaves MP (1982) Effects of pesticides on soil microorganisms. In: Burns RG, Slater JH (eds) Experimental Microbial Ecology. Blackwell, Oxford, pp 613–630

    Google Scholar 

  • Haney RL, Senseman SA, Krutz LJ, Hons FM (2002) Soil carbon and nitrogen mineralization as affected by atrazine and glyphosate. Biol Fertil Soils 35:35–40

    Article  CAS  Google Scholar 

  • Hart MR, Brookes PC (1997) Soil microbial biomass and mineralisation of soil organic matter after 19 years of cumulative field applications of pesticides. Soil Biol Biochem 28:1641–1649

    Article  Google Scholar 

  • Herwig U, Klumpp E, Narres H-D, Schwuger MJ (2001) Physicochemical interactions between atrazine and clay minerals. Appl Clay Sci 18:211–222

    Article  CAS  Google Scholar 

  • Hussain S, Siddique T, Saleem M, Arshad M, Khalid A (2009) Impact of pesticides on soil microbial diversity, enzymes, and biochemical reactions. Adv Agron 22:159–200

    Article  Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72

    Article  CAS  Google Scholar 

  • Kaufman DD, Kearney PC (1970) Microbial degradation of s-triazine herbicides. Res Rev 32:235–265

    CAS  Google Scholar 

  • Koskinen WC, Clay SA (1998) Factors affecting atrazine rate in North Central U.S. Soils. Rev Environ Contam Toxicol 151:117–165

    Google Scholar 

  • Kruglow JW, Gersz NB, Piercewa AN, Bay-Bienko NW, Michajlowa EI (1974) The effect of long-term herbicide application on microflora and some biochemical processes in soil. Roczniki Gleboznawcze 26:159–164

    Google Scholar 

  • Mahía J, Díaz-Raviña M (2007) Atrazine degradation and residues distribution in two acid soils from temperate humid zone. J Environ Qual 36:826–831

    Article  PubMed  Google Scholar 

  • Mahía J, Martín A, Carballas T, Díaz-Raviña M (2007) Atrazine degradation and enzyme activities in an agricultural soil under two tillage systems. Sci Total Environ 378:187–194

    Article  PubMed  Google Scholar 

  • Mahía J, Cabaneiro A, Carballas T, Díaz-Raviña M (2008a) Microbial biomass and C mineralization in agricultural soil as affected by atrazine addition. Biol Fertil Soils 45:99–105

    Article  Google Scholar 

  • Mahía J, Martín A, Díaz-Raviña M (2008b) Extractable atrazine and its metabolites in agricultural soils from temperate humid zone. Environ Geochem Health 30:147–152

    Article  PubMed  Google Scholar 

  • Mandelbaum RT, Wackett LP, Allan DL (1993) Mineralization of the s-triazine ring of atrazine by stable bacterial mixed cultures. Appl Environ Microbiol 69:1695–1701

    Google Scholar 

  • Mandelbaum RT, Allan DL, Wackett LP (1995) Isolation and characterization of a Pseudomonas sp. that mineralizes the s-triazine herbicide atrazine. Appl Environ Microbiol 61:1451–1457

    PubMed  CAS  Google Scholar 

  • Moreno JL, Aliaga A, Navarro S, Hernández T, García C (2007) Effects of atrazine on microbial activity in semiarid soil. Appl Soil Ecol 35:120–127

    Article  Google Scholar 

  • Nannipieri P (1994) The potential use of soil enzymes as indicators of productivity, sustainability and pollution. In: Pankurst CE, Doube BM, Gupta VVSR, Grace PR (eds) Soil Biota: Management in Sustainable Farming Systems. CSIRO, Melbourne East, pp 238–244

    Google Scholar 

  • Ostrofsky EB, Robinson JB, Traina SJ, Tuovinen OH (2002) Analysis of atrazine-degrading microbial communities in soils using most-probable-number enumeration, DNA hybridization, and inhibitors. Soil Biol Biochem 34:1449–1459

    Article  CAS  Google Scholar 

  • Perucci C, Dummontet S, Mazzatura A (2000) Effects of organic amendment and herbicide treatment on soil microbial biomass. Biol Fertil Soils 32:17–23

    Article  CAS  Google Scholar 

  • Puget P, Angers DA, Chenu C (1999) Nature of carbohydrates associated with water-stable aggregates of two cultivated soils. Soil Biol Biochem 31:55–63

    Article  CAS  Google Scholar 

  • Radosevich M, Traina SJ, Hao L, Tuovinen OH (1995) Degradation and mineralization of atrazine by a soil bacterial isolate. Appl Environ Microbiol 61:297–302

    PubMed  CAS  Google Scholar 

  • Rhine ED, Fuhrmann JJ, Radosevich M (2003) Microbial community responses to atrazine exposure and nutrient availability: linking degradation capacity to community structure. Microbial Ecol 46:145–160

    Article  CAS  Google Scholar 

  • Ross M, Goberna M, Moreno JL, Hernández T, García C, Insam H, Pascual JA (2006) Molecular and physiological bacterial diversity of a semiarid soil contaminated with different levels of formulated atrazine. Appl Soil Ecol 34:93–102

    Article  Google Scholar 

  • Rousseaux S, Hartmann A, Soulas G (2001) Isolation and characterisation of new Gram-negative and Gram-positive atrazine degrading bacteria from different French soils. FEMS Microbiol Ecol 36:211–222

    Article  PubMed  CAS  Google Scholar 

  • Sannino F, Gianfreda L (2001) Pesticide influence on soil enzymatic activities. Chemosphere 45:417–425

    Article  PubMed  CAS  Google Scholar 

  • Schaëfer A (1993) Pesticide effects on enzyme activities in the soil ecosystem. In: Bollag JM, Stotzky G (eds) Soil Biochemistry Vol. 8. Marcel Dekker, New York, pp 273–371

    Google Scholar 

  • Schiavon M (1988) Studies of the leaching of atrazine, of its chlorinated derivatives, and of hydroxyatrazine from soil using 14C ring-labelled compounds under outdoor conditions. Ecotoxicol Environ Saf 15:46–54

    Article  PubMed  CAS  Google Scholar 

  • Seghers D, Verthé K, Reheul D, Bulcke R, Siciliano SD, Vertraete W, Top EM (2003) Effect of long-term herbicide applications on the bacterial community structure and function in an agricultural soil. FEMS Microbiol Ecol 46:139–146

    Article  PubMed  CAS  Google Scholar 

  • Topp E, Vallaeys T, Soulas G (1997) Pesticides: microbial degradation and effects on soil microorganisms. In: van Elsas JD, Trevors JT, Wellington EMH (eds) Modern Soil Microbiology. Marcel Dekker, New York, pp 547–575

    Google Scholar 

  • Voets JP, Meerschman P, Verstraete W (1974) Soil microbiological and biochemical effects of long-term atrazine applications. Soil Biol Biochem 6:149–152

    Article  CAS  Google Scholar 

  • Yanze-Kontchou C, Gschwind N (1994) Mineralization of the herbicide atrazine as a carbon source by a Pseudomonas strain. Appl Environ Microbiol 60:4297–4302

    PubMed  CAS  Google Scholar 

  • Yassir A, Rie C, Soulas G (1998) Microbial N-Dealkylation of atrazine: effect of exogenous organic substrates and behaviour of the soil microflora. Pest Sci 54:75–82

    Article  CAS  Google Scholar 

  • Yassir A, Lagacherie B, Houot S, Soulas G (1999) Microbial aspects of atrazine biodegradation in relation to history of soil treatment. Pest Sci 55:799–809

    Article  CAS  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterization of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Marcos Godoy Iglesias for the technical assistance. This study was supported by the Secretaría Xeral de Investigación e Desenvolvemento da Xunta de Galicia (Project PGIDT01PXI40002PR) and by Spanish Ministerio de Ciencia y Tecnología (Project AGL2005-05726-C02-01).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Montserrat Díaz-Raviña.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mahía, J., González-Prieto, S.J., Martín, A. et al. Biochemical properties and microbial community structure of five different soils after atrazine addition. Biol Fertil Soils 47, 577–589 (2011). https://doi.org/10.1007/s00374-011-0569-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-011-0569-x

Keywords

Navigation