Skip to main content

Advertisement

Log in

Mineralization of s-triazine herbicides by a newly isolated Nocardioides species strain DN36

  • Environmental Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

A novel s-triazine-mineralizing bacterium—Nocardioides sp. strain DN36—was isolated from paddy field soil treated with ring-U-14C-labeled simetryn ([14C]simetryn) in a model paddy ecosystem (microcosm). In a tenfold-diluted R2A medium, strain DN36 liberated 14CO2 from not only [14C]simetryn but also three ring-U-14C-labeled s-triazines: atrazine, simazine, and propazine. We found that DN36 mineralized ring-U-14C–cyanuric acid added as an initial substrate, indicating that the bacterium mineralized s-triazine herbicides via a common metabolite, namely, cyanuric acid. Strain DN36 harbored a set of genes encoding previously reported s-triazine-degrading enzymes (TrzN-AtzB-AtzC), and it also transformed ametryn, prometryn, dimethametryn, atraton, simeton, and prometon. The findings suggest that strain DN36 can mineralize a diverse range of s-triazine herbicides. To our knowledge, strain DN36 is the first Nocardioides strain that can individually mineralize s-triazine herbicides via the ring cleavage of cyanuric acid. Further, DN36 could not grow on cyanuric acid, and the degradation seemed to occur cometabolically.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aislabie J, Bej AK, Ryburn J, Lloyd N, Wilkins A (2005) Characterization of Arthrobacter nicotinovorans HIM, an atrazine-degrading bacterium, from agricultural soil New Zealand. FEMS Microbiol Ecol 52:279–286

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Behki R, Topp E, Dick W, Germon P (1993) Metabolism of the herbicide atrazine by Rhodococcus strains. Appl Environ Microbiol 59:1955–1959

    CAS  Google Scholar 

  • Boundy-Mills KL, de Souza ML, Mandelbaum RT, Wackett LP, Sadowsky MJ (1997) The atzB gene of Pseudomonas sp. strain ADP encodes the second enzyme of a novel atrazine degradation pathway. Appl Environ Microbiol 63:916–923

    CAS  Google Scholar 

  • Cai B, Han Y, Liu B, Ren Y, Jiang S (2003) Isolation and characterization of an atrazine-degrading bacterium from industrial wastewater in China. Lett Appl Microbiol 36:272–276

    Article  CAS  Google Scholar 

  • Coleman NV, Mattes TE, Gossett JM, Spain JC (2002) Phylogenetic and kinetic diversity of aerobic vinyl chloride-assimilating bacteria from contaminated sites. Appl Environ Microbiol 68:6162–6171

    Article  CAS  Google Scholar 

  • de Souza ML, Sadowsky MJ, Wackett LP (1996) Atrazine chlorohydrolase from Pseudomonas sp. strain ADP: gene sequence, enzyme purification, and protein characterization. J Bacteriol 178:4894–4900

    Google Scholar 

  • de Souza ML, Seffernick J, Martinez B, Sadowsky MJ, Wackett LP (1998) The atrazine catabolism genes atzABC are widespread and highly conserved. J Bacteriol 180:1950–1954

    Google Scholar 

  • Devereux R, Wilkinson SS (2004) Amplification of ribosomal RNA sequences. In: Kowalchuk GA, de Bruijn FJ, Head IM, Akkermans ADL, van Elsas JD (eds) Molecular microbial ecology manual, 2nd edn. Kluwer Academic Publishers, Netherlands, pp 509–522

    Google Scholar 

  • Devers M, Azhari NE, Kolic NU, Martin-Laurent F (2007) Detection and organization of atrazine-degrading genetic potential of seventeen bacterial isolates belonging to divergent taxa indicate a recent common origin of their catabolic functions. FEMS Microbiol Lett 273:78–86

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fruchey I, Shapir N, Sadowsky MJ, Wackett LP (2003) On the origins of cyanuric acid hydrolase: purification, substrates, and prevalence of AtzD from Pseudomonas sp. strain ADP. Appl Environ Microbiol 69:3653–3657

    Article  CAS  Google Scholar 

  • Fujii K, Takagi K, Hiradate S, Iwasaki A, Harada N (2007) Biodegradation of methylthio-s-triazines by Rhodococcus sp. strain FJ1117YT, and production of the corresponding methylsulfinyl, methylsulfonyl and hydroxyl analogues. Pest Manag Sci 63:254–260

    Article  CAS  Google Scholar 

  • Getenga Z, Dörfler U, Iwobi A, Schmid M, Schroll R (2009) Atrazine and terbuthylazine mineralization by an Arthrobacter sp. isolated from a sugarcane-cultivated soil in Kenya. Chemosphere 77:534–539

    Article  CAS  Google Scholar 

  • Hernández M, Villalobos P, Morgante V, González M, Reiff C, Moore E, Seeger M (2008) Isolation and characterization of a novel simazine-degrading bacterium from agricultural soil of central Chili, Pseudomonas sp. MHP41. FEMS Microbiol Lett 286:184–190

    Article  Google Scholar 

  • Iwasaki A, Takagi K, Yoshioka Y, Fujii K, Kojima Y, Harada N (2007) Isolation and characterization of a novel simazine-degrading β-proteobacterium and detection of genes encoding s-triazine-degrading enzymes. Pest Manag Sci 63:261–268

    Article  CAS  Google Scholar 

  • Karns JS (1999) Gene sequence and properties of an s-triazine ring-cleavage enzyme from Pseudomonas sp. strain NRRLB-12227. Appl Environ Microbiol 65:3512–3517

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Korpraditskul R, Katayama A, Kuwatsuka S (1993) Degradation of atrazine by soil bacteria in the stationary phase. J Pestic Sci 18:293–298

    CAS  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

    CAS  Google Scholar 

  • Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218

    Article  CAS  Google Scholar 

  • Martinez B, Tomkins J, Wackett LP, Wing R, Sadowsky MJ (2001) Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol 183:5684–5697

    Article  CAS  Google Scholar 

  • Mulbry WM, Zhu H, Nour SM, Topp E (2002) The triazine hydrolase gene trzN from Nocardioides sp. strain C190: cloning and construction of gene-specific primers. FEMS Microbiol Lett 206:75–79

    Article  CAS  Google Scholar 

  • Nagy I, Compernolle F, Ghys K, Jos V, De Mot R (1995) A single cytochrome P-450 system is involved in degradation of the herbicides EPTC (s-ethyl dipropylthiocarbamate) and atrazine by Rhodococcus sp. strain NI86/21. Appl Environ Microbiol 61:2056–2060

    CAS  Google Scholar 

  • Piutti S, Semon E, Landry D, Hartmann A, Dousset S, Lichtfouse E, Topp E, Soulas G, Martin-Laurent F (2003) Isolation and characterization of Nocardioides sp. SP12, an atrazine-degrading bacterial strain possessing the gene trzN from bulk and maize rhizosphere soil. FEMS Microbiol Lett 221:111–117

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sadowsky MJ, Tong Z, de Souza ML, Wackett LP (1998) AtzC is a new member of the amidohydrolase protein superfamily and is homologous to other atrazine-metabolizing enzymes. J Bacteriol 180:152–158

    CAS  Google Scholar 

  • Sajjaphan K, Shapir N, Wackett LP, Palmer M, Blackmon B, Tomkins J, Sadowsky MJ (2004) Arthrobacter aurescens TC1 atrazine catabolism genes trzN, atzB, and atzC are linked on a 160-kilobase region and are functional in Escherichia coli. Appl Environ Microbiol 70:4402–4407

    Article  CAS  Google Scholar 

  • Satsuma K (2006) Characterisation of new strains of atrazine-degrading Nocardioides sp. isolated from Japanese riverbed sediment using naturally derived river ecosystem. Pest Manag Sci 62:340–349

    Article  CAS  Google Scholar 

  • Shapir N, Rosendahl C, Johnson G, Andreina M, Sadowsky MJ, Wackett LP (2005) Substrate specificity and colorimetric assay for recombinant TrzN derived from Arthrobacter aurescens TC1. Appl Environ Microbiol 71:2214–2220

    Article  CAS  Google Scholar 

  • Shapir N, Mongodin EF, Sadowsky MJ, Daugherty SC, Nelson KE, Wackett LP (2007) Evolution of catabolic pathways: genomic insights into microbial s-triazine metabolism. J Bacteriol 189:674–682

    Article  CAS  Google Scholar 

  • Skipper HD, Volk VV (1972) Biological and chemical degradation of atrazine in three Oregon soils. Weed Sci 20:344–347

    CAS  Google Scholar 

  • Strong LC, Rosendahl C, Johnson G, Sadowsky MJ, Wackett LP (2002) Arthrobacter aurescens TC1 metabolizes diverse s-triazine ring compounds. Appl Environ Microbiol 68:5973–5980

    Article  CAS  Google Scholar 

  • Struthers JK, Jayachandran K, Moorman TB (1998) Biodegradation of atrazine by Agrobacterium radiobacter J14a and use of this strain in bioremediation of contaminated soil. Appl Environ Microbiol 64:3368–3375

    CAS  Google Scholar 

  • Topp E, Mulbry WM, Zhu H, Nour SM, Cuppels D (2000a) Characterization of s-triazine herbicide metabolism by a Nocardioides sp. isolated from agricultural soils. Appl Environ Microbiol 66:3134–3141

    Article  CAS  Google Scholar 

  • Topp E, Zhu H, Nour SM, Houot S, Lewis M, Cuppels D (2000b) Characterization of an atrazine-degrading Pseudamonobacter sp. isolated from Canadian and French agricultural soils. Appl Environ Microbiol 66:2773–2782

    Article  CAS  Google Scholar 

  • Vargha M, Takáts Z, Márialigeti K (2005) Degradation of atrazine in a laboratory scale model system with Danube river sediment. Water Res 39:1560–1568

    Article  CAS  Google Scholar 

  • Vibber LL, Pressler MJ, Colores GM (2007) Isolation and characterization of novel atrazine-degrading microorganisms from an agricultural soil. Appl Microbiol Biotechnol 75:921–928

    Article  CAS  Google Scholar 

  • Yamazaki K, Fujii K, Iwasaki A, Takagi K, Satsuma K, Harada N, Uchimura Y (2008) Different substrate specificities of two triazine hydrolases (TrzNs) from Nocardioides species. FEMS Microbiol Lett 286:171–177

    Article  CAS  Google Scholar 

Download references

Acknowledgements

I am grateful to Nippon Kayaku Co. Ltd. for providing radiolabeled simetryn. I am also grateful to Dr Kazuhiro Takagi for providing the DNA extract of the simazine-degrading β-proteobacterium. I wish to thank Minoru Masuda and Aiko Kamogawa for their excellent technical assistance and Dr. Kiyoshi Sato and Dr. Yasuhiro Kato for their kind advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Koji Satsuma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Satsuma, K. Mineralization of s-triazine herbicides by a newly isolated Nocardioides species strain DN36. Appl Microbiol Biotechnol 86, 1585–1592 (2010). https://doi.org/10.1007/s00253-010-2460-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-010-2460-3

Keywords