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Isolation and characterization of Bradyrhizobium sp. SR1 degrading two β-triketone herbicides

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Abstract

In this study, a bacterial strain able to use sulcotrione, a β-triketone herbicide, as sole source of carbon and energy was isolated from soil samples previously treated with this herbicide. Phylogenetic study based on16S rRNA gene sequence showed that the isolate has 100 % of similarity with several Bradyrhizobium and was accordingly designated as Bradyrhizobium sp. SR1. Plasmid profiling revealed the presence of a large plasmid (>50 kb) in SR1 not cured under nonselective conditions. Its transfer to Escherichia coli by electroporation failed to induce β-triketone degrading capacity, suggesting that degrading genes possibly located on this plasmid cannot be expressed in E. coli or that they are not plasmid borne. The evaluation of the SR1 ability to degrade various synthetic (mesotrione and tembotrione) and natural (leptospermone) triketones showed that this strain was also able to degrade mesotrione. Although SR1 was able to entirely dissipate both herbicides, degradation rate of sulcotrione was ten times higher than that of mesotrione, showing a greater affinity of degrading-enzyme system to sulcotrione. Degradation pathway of sulcotrione involved the formation of 2-chloro-4-mesylbenzoic acid (CMBA), previously identified in sulcotrione degradation, and of a new metabolite identified as hydroxy-sulcotrione. Mesotrione degradation pathway leads to the accumulation of 4-methylsulfonyl-2-nitrobenzoic acid (MNBA) and 2-amino-4 methylsulfonylbenzoic acid (AMBA), two well-known metabolites of this herbicide. Along with the dissipation of β-triketones, one could observe the decrease in 4-hydroxyphenylpyruvate dioxygenase (HPPD) inhibition, indicating that toxicity was due to parent molecules, and not to the formed metabolites. This is the first report of the isolation of bacterial strain able to transform two β-triketones.

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Acknowledgments

This work was supported by the French “Agence National de la Recherche” under TRICETOX project, number ANR-13-CESA-0002. Leptospermone was kindly provided by Franck E. Dayan (Natural Products Utilization Research Unit, USDA). The authors would like to thank Nathalie Bontemps (LCBE-CRIOBE-USR 3278 CNRS EPHE, UPVD) for sulcotrione metabolite analysis. The authors declare that they have no conflict of interest. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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All authors agreed to be listed and have approved of the manuscript, its content, and its submission to Environmental Science and Pollution Research. It has not been submitted or published elsewhere, whether partly or fully. All authors are in agreement with the ethical rules of ESPR.

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Authors and Affiliations

  1. Biocapteurs Analyses Environnement (BAE), University of Perpignan Via Domitia, 66860, Perpignan, France

    Sana Romdhane, Emilie Rocaboy-Faquet & Lise Barthelmebs

  2. Laboratoire de Chimie des Biomolécules et de l’Environnement–CRIOBE–USR 3278 CNRS EPHE, University of Perpignan Via Domitia, 66860, Perpignan, France

    Sana Romdhane, Christophe Calvayrac & Jean-François Cooper

  3. INRA, UMR 1347 Agroécologie, Pole Ecoldur, 17 rue Sully, BP 86510, 21065, Dijon Cedex, France

    Sana Romdhane, Marion Devers-Lamrani & Fabrice Martin-Laurent

  4. INPT, ENSIACET, Université de Toulouse, 31432, Toulouse, France

    David Riboul

  5. Laboratoire de Génie Chimique (LGC UMR 5503), CNRS, 4 allée Emile Monso, BP 84234, 31432, Toulouse, France

    David Riboul

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  1. Sana Romdhane
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  2. Marion Devers-Lamrani
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Correspondence to Lise Barthelmebs.

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Supplementary data Fig. 1

Degradation curves of triketone herbicides by Bradyrhizobium sp. SR1 in resting cell experiments. a Degradation of sulcotrione at 35 mg L−1 (106 μM) and appearance of CMBA expressed in μM. Transitory accumulation of hydroxy-sulcotrione in the medium is represented in arbitrary unit. b Degradation of mesotrione at 35 mg L−1 (103 μM) and accumulation of MNBA and AMBA in the medium. Standard deviations are indicated (n = 3). (PPTX 78 kb)

Supplementary data Fig. 2

Proposed scheme for mesotrione metabolic pathway of Bradyrhizobium sp. SR1 and Bacillus sp. 3B6. SR1 (1) Mesotrione is transformed into MNBA and AMBA within two different pathways. SR1 (2) Mesotrione is first transformed into MNBA, which is then transformed into AMBA. Dashed arrows indicate hypothetical degradation pathway. 3B6 (1) Major pathway of mesotrione degradation. 3B6 (2) Minor pathway of mesotrione degradation from Durand et al. 2010. (PPTX 157 kb)

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Romdhane, S., Devers-Lamrani, M., Martin-Laurent, F. et al. Isolation and characterization of Bradyrhizobium sp. SR1 degrading two β-triketone herbicides. Environ Sci Pollut Res 23, 4138–4148 (2016). https://doi.org/10.1007/s11356-015-4544-1

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