Abstract
Bioherbicides appear as an ecofriendly alternative to synthetic herbicides, generally used for weed management, because they are supposed to have low side on human health and ecosystems. In this context, our work aims to study abiotic (i.e., photolysis) and biotic (i.e,. biodegradation) processes involved in the fate of leptospermone, a natural β-triketone herbicide, by combining chemical and microbiological approaches. Under controlled conditions, the photolysis of leptospermone was sensitive to pH. Leptospermone has a half-life of 72 h under simulated solar light irradiations. Several transformation products, including hydroxy-leptospermone, were identified. For the first time, a bacterial strain able to degrade leptospermone was isolated from an arable soil. Based on its 16S ribosomal RNA (rRNA) gene sequence, it was affiliated to the Methylophilus group and was accordingly named as Methylophilus sp. LS1. Interestingly, we report that the abundance of OTUs, similar to the 16S rRNA gene sequence of Methylophilus sp. LS1, was strongly increased in soil treated with leptospermone. The leptospermone was completely dissipated by this bacteria, with a half-life time of 6 days, allowing concomitantly its growth. Hydroxy-leptospermone was identified in the bacterial culture as a major transformation product, allowing us to propose a pathway of transformation of leptospermone including both abiotic and biotic processes.
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References
Awata H, Endo F, Matsuda I (1994) Structure of the human 4-hydroxyphenylpyruvic acid dioxygenase gene (HPD). Genomics 23:534–539
Bardot C et al (2015) How the edaphic Bacillus megaterium strain Mes11 adapts its metabolism to the herbicide mesotrione pressure. Environ Pollut 199:198–208
Bartley GE, Maxwell CA, Wittenbach VA, Scolnik PA (1997) Cloning of an Arabidopsis thaliana cDNA for p-hydroxyphenylpyruvate dioxygenase (Accession No. U89267)
Beaudegnies R et al (2009) Herbicidal 4-hydroxyphenylpyruvate dioxygenase inhibitors-a review of the triketone chemistry story from a Syngenta perspective. Bioorg Med Chem 17:4134–4152
Bonnet JL, Bonnemoy F, Dusser M, Bohatier J (2008) Toxicity assessment of the herbicides sulcotrione and mesotrione toward two reference environmental microorganisms: Tetrahymena pyriformis and Vibrio fischeri. Arch Environ Contam Toxicol 55:576–583
Busse MD, Ratcliff AW, Shestak CJ, Powers RF (2001) Glyphosate toxicity and the effects of long-term vegetation control on soil microbial communities. Soil Biol Biochem 33:1777–1789
Calvayrac C, Bontemps N, Nouga-Bissoue A, Romdhane S, Coste C-M, Cooper J-F (2013) Photolysis of tembotrione and its main by-products under extreme artificial conditions: comparison with another beta-triketone herbicide. Sci Total Environ 452:227–232
Calvayrac C et al (2012) Isolation and characterisation of a bacterial strain degrading the herbicide sulcotrione from an agricultural soil. Pest Manag Sci 68:340–347
Cantrell CL, Dayan FE, Duke SO (2012) Natural products as sources for new pesticides. J Nat Prod 75:1231–1242
Carles L, Besse-Hoggan P, Joly M, Vigouroux A, Morera S, Batisson I (2016) Functional and structural characterization of two Bacillus megaterium nitroreductases biotransforming the herbicide mesotrione. Biochem J 473:1443–1453
Chaabane H, Cooper JF, Azouzi L, Coste CM (2005) Influence of soil properties on the adsorption-desorption of sulcotrione and its hydrolysis metabolites on various soils. J Agric Food Chem 53:4091–4095
Chaabane H, Vulliet E, Joux F, Lantoine F, Conan P, Cooper J-F, Coste C-M (2007) Photodegradation of sulcotrione in various aquatic environments and toxicity of its photoproducts for some marine micro-organisms. Water Res 41:1781–1789
Chaabane H, Vulliet E, Calvayrac C, Coste C-M, Cooper J-F (2008) Behaviour of sulcotrione and mesotrione in two soils. Pest Manag Sci 64:86–93
Crouzet O et al (2010) Response of soil microbial communities to the herbicide mesotrione: a dose-effect microcosm approach. Soil Biol Biochem 42:193–202
Dayan FE, Duke SO, Sauldubois A, Singh N, McCurdy C, Cantrell C (2007) P-Hydroxyphenylpyruvate dioxygenase is a herbicidal target site for beta-triketones from Leptospermum scoparium. Phytochemistry 68:2004–2014
Dayan FE, Cantrell C, Duke SO (2009) Natural products in crop protection. Bioorg Med Chem 17:4022–4034
Dayan FE, Howell JL, Marais JP, Ferreira D, Koivunen M (2011) Manuka oil, a natural herbicide with preemergence activity. Weed Sci 59:464–469
De Marco P, Pacheco CC, Figueiredo AR, Moradas-Ferreira P (2004) Novel pollutant-resistant methylotrophic bacteria for use in bioremediation. FEMS Microbiol Lett 234:75–80
Denoya CD, Skinner DD, Morgenstern MR (1994) A streptomyces-avermitilis gene enconding a 4-ydroxypenlpyruvic acid dioxygenase-like protein that directs the production of homogentisic acid and an ochronotic pigment in Escherichia coli. J Bacteriol 176:5312–5319
Douglas MH, van Klink JW, Smallfield BM, Perry NB, Anderson RE, Johnstone P, Weavers RT (2004) Essential oils from New Zealand manuka: triketone and other chemotypes of Leptospermum scoparium. Phytochemistry 65:1255–1264
El Sebai T, Lagacherie B, Soulas G, Martin-Laurent F (2004) Isolation and characterisation of an isoproturon-mineralising Methylopila sp. TES from French agricultural soil. FEMS Microbiol Lett 239:103–110
Eyice O, Namura M, Chen Y, Mead A, Samavedam S, Schafer H (2015) SIP metagenomics identifies uncultivated Methylophilaceae as dimethylsulphide degrading bacteria in soil and lake sediment. ISME J 9:2336–2348
Garcia I, Rodgers M, Lenne C, Rolland A, Sailland A, Matringe M (1997) Subcellular localization and purification of a p-hydroxyphenylpyruvate dioxygenase from cultured carrot cells and characterization of the corresponding cDNA. Biochem J 325:761–769
Gogleva AA, Kaparullina EN, DoroninaNina V, Ao TY (2010) Methylophilus flavus sp. nov. and Methylophilus luteus sp. nov., aerobic, methylotrophic bacteria associated with plants. Int J Syst Evol Microbiol 60:2623–2628
Gopal M, Gupta A, Arunachalam V, Magu SP (2007) Impact of azadirachtin, an insecticidal allelochemical from neem on soil microflora, enzyme and respiratory activities. Bioresour Technol 98:3154–3158
Gürtler V1, and Stanisich VA (1996) New approaches to typing and identification of bacteria using the 16S–23S rDNA spacer region. Microbiology 142:3-16
Gray R, Tseng C, Rusay R (1980) 1-Hydroxy-2-(alkylketo)-4,4,6,6-tetramethyl cyclohexen-3,5-dione herbicides. US Patent 4,202,840
Hellyer RO (1968) The occurrence of β-triketones in the steam-volatile oils of some myrtaceous Australian plants. Aust J Chem 21:2825–2828
Joly P, Bonnemoy F, Charvy JC, Bohatier J, Mallet C (2013) Toxicity assessment of the maize herbicides S-metolachlor, benoxacor, mesotrione and nicosulfuron, and their corresponding commercial formulations, alone and in mixtures, using the Microtox® test. Chemosphere 93:2444–2450
Kök FN, Arıca MY, Halıcıgil C, Alaeddinoglu G, Hasırcı V (1999) Biodegradation of aldicarb in a packed-bed reactor by immobilized Methylosinus. Enzym Microb Technol 24:291–296
Lapidus A et al (2011) Genomes of three methylotrophs from a single niche reveal the genetic and metabolic divergence of the Methylophilaceae. J Bacteriol 193:3757–3764
Letunic I, Bork P (2007) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478
Meazza G et al (2002) The inhibitory activity of natural products on plant p-hydroxyphenylpyruvate dioxygenase. Phytochemistry 60:281–288
Mitchell G, Bartlett DW, Fraser TEM, Hawkes TR, Holt DC, Townson JK, Wichert RA (2001) Mesotrione: a new selective herbicide for use in maize. Pest Manag Sci 57:120–128
Nagy I, Compernolle F, Ghys K, Vanderleyden J, 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
O’Sullivan J, Van Acker R, Grohs R, Riddle R (2015) Improved herbicide efficacy for organically grown vegetables. Org Agr 4:315–322
Olchanheski LR et al (2014) Mechanisms of tolerance and high degradation capacity of the herbicide mesotrione by Escherichia coli strain DH5-α. Plos One 9. doi:10.1371/journal.pone.0099960
Owens DK, Nanayakkara NPD, Dayan FE (2013) In planta mechanism of action of leptospermone: impact of its physico-chemical properties on uptake, translocation, and metabolism. J Chem Ecol 39:262–270
Patil C et al (2016) Environmental Metabolic Footprinting: a novel application to study the impact of a natural and a synthetic beta-triketone herbicide in soil. Sci Total Environ 566-567:552–558
Perriere G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369
Piutti S et al (2003) Isolation and characterisation 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
Rocaboy-Faquet E, Noguer T, Romdhane S, Bertrand C, Dayan FE, Barthelmebs L (2014) Novel bacterial bioassay for a high-throughput screening of 4-hydroxyphenylpyruvate dioxygenase inhibitors. Appl Microbiol Biotechnol 98:7243–7252
Romdhane S et al (2016) Ecotoxicological impact of the bioherbicide leptospermone on the microbial community of two arable soils. Front Microbiol 7:775
Romdhane S et al (2015) Isolation and characterization of Bradyrhizobium sp. SR1 degrading two β-triketone herbicides. Environ Sci Pollut Res Int 23:4138–4148
Ros M, Goberna M, Moreno JL, Hernandez T, Garcia C, Insam H, Pascual JA (2006) Molecular and physiological bacterial diversity of a semi-arid soil contaminated with different levels of formulated atrazine. Appl Soil Ecol 34:93–102
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
Ruetschi U, Dellsen A, Sahlin P, Stenman G, Rymo L, Lindstedt S (1993) Human 4-hydroxphenylpyruvate dioxygenase—primary structure and chromosomal localization of the gene. Eur J Biochem 213:1081–1089
Ruetschi U, Odelhoeg B, Lindstedt S, Barros-Soderling J, Persson B, Joernvall H (1992) Characterization of 4-hydroxyphenylpyruvate dioxygenase. Primary structure of the Pseudomonas gene. Eur J Biochem 205:459–466
Schulz A, Ort O, Beyer P, Kleinig H (1993) SC-0051, a 2-benzoyl-cyclohexane-1,3-dione bleaching herbicide, is a potent inhibitor of the enzyme p-hydroxyphenylpyruvate dioxygenase. FEBS Lett 318:162–166
Siehl DL et al (2014) Broad 4-hydroxyphenylpyruvate dioxygenase inhibitor herbicide tolerance in soybean with an optimized enzyme and expression cassette. Plant Physiol 166:1162–1176
Singh S, Gupta R, Kumari M, Sharma S (2015) Nontarget effects of chemical pesticides and biological pesticide on rhizospheric microbial community structure and function in Vigna radiata. Environ Sci Pollut Res 22:11290–11300
Ter Halle A, Richard C (2006) Simulated solar light irradiation of mesotrione in natural waters. Environ Sci Technol 40:3842–3847
Ter Halle A, Wiszniowski J, Richard C (2007) Phototransformation of pesticides on plant leaves: the case of sulcotrione. Commun Agric Appl Biol Sci 72:45–52
Ter Halle A et al (2009) Photolysis of the herbicide sulcotrione: formation of a major photoproduct and its toxicity evaluation. Pest Manag Sci 65:14–18
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Trivella A, Stawinoga M, Dayan FE, Cantrell CL, Mazellier P, Richard C (2015) Photolysis of natural beta-triketonic herbicides in water. Water Res 78:28–36
van Klink JW et al (2005) Triketones active against antibiotic-resistant bacteria: synthesis, structure-activity relationships, and mode of action. Bioorg Med Chem 13:6651–6662
Weaver MA, Krutz LJ, Zablotowicz RM, Reddy KN (2007) Effects of glyphosate on soil microbial communities and its Mississippi soil. Pest Manag Sci 63:388–393
Weir TL, Park SW, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479
Wiszniowski J, Halle AT, Richard C, Hitmi A, Ledoigt G (2009) Photodegradation product of sulcotrione and the physiological response of maize (Zea mays) and white mustard (Sinapis alba). Chemosphere 74:1224–1230
Wu N et al (2011) Effects of sulcotrione [2-(2-chloro-4-mesylbenzoyl)-cyclohexane-1,3-dione] on enzymes involved in tyrosine catabolism and the extent of the resulting tyrosinemia and its relationship with corneal lesions in rats. Pestic Biochem Physiol 99:162–169
Wyckoff EE, Pishko EJ, Kirkland TN, Cole GT (1995) Cloning and expression of a gene encoding a T-cell reactive protein from coccidioides immitis to 4-hydrophenylpyruvate dioxygenase ad the mammalian F antigen. Gene 161:107–111
Zhang S-y , Wang Q-f, Wan R, Xie S-g (2011) Changes in bacterial community of anthracene bioremediation in municipal solid waste composting soil. J Zhejiang Univ Sci B 12:760–768
Zwietering MH, Jongenburger I, Rombouts FM, Riet KV (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881
Acknowledgments
This work was supported by the “Agence National de la Recherche” under TRICETOX project, number ANR-13-CESA-0002. The authors would like to thank David Riboul (INPT, ENSIACET, Université de Toulouse) for helpful analysis.
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Romdhane, S., Devers-Lamrani, M., Martin-Laurent, F. et al. Evidence for photolytic and microbial degradation processes in the dissipation of leptospermone, a natural β-triketone herbicide. Environ Sci Pollut Res 25, 29848–29859 (2018). https://doi.org/10.1007/s11356-017-9728-4
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Keywords
- Bioherbicides
- Leptospermone
- Photodegradation
- Biodegradation
- Transformation products
- Methylophilus sp. LS1