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.


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
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
Behki R, Topp E, Dick W, Germon P (1993) Metabolism of the herbicide atrazine by Rhodococcus strains. Appl Environ Microbiol 59:1955–1959
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
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
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
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
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
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
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
Erickson LE, Lee KH (1989) Degradation of atrazine and related s-triazines. Crit Rev Environ Control 19:1–14
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
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
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
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
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
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
Kaufman DD, Kearney PC (1970) Microbial degradation of s-triazine herbicides. Residue Rev 32:235–265
Korpraditskul R, Katayama A, Kuwatsuka S (1993) Degradation of atrazine by soil bacteria in the stationary phase. J Pestic Sci 18:293–298
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
Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–218
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
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
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
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
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
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
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
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
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
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
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
Skipper HD, Volk VV (1972) Biological and chemical degradation of atrazine in three Oregon soils. Weed Sci 20:344–347
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
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
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
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
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
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
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
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
Corresponding author
Rights 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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-010-2460-3


