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Impact of Leptospermone, a Natural -Triketone Herbicide, on the Fungal

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Impact of Leptospermone, a Natural -Triketone Herbicide, on the Fungal Impact of Leptospermone, a Natural β-Triketone Herbicide, on the Fungal Composition and Diversity of Two Arable Soils Clarisse Mallet, Sana Romdhane, Camille Loiseau, Jérémie Béguet, Fabrice Martin-Laurent, Christophe Calvayrac, Lise Barthelmebs To cite this version: Clarisse Mallet, Sana Romdhane, Camille Loiseau, Jérémie Béguet, Fabrice Martin-Laurent, et al.. Impact of Leptospermone, a Natural β-Triketone Herbicide, on the Fungal Composition and Diversity of Two Arable Soils. Frontiers in Microbiology, Frontiers Media, 2019, 10, 10.3389/fmicb.2019.01024. hal-02143873 HAL Id: hal-02143873 https://hal.sorbonne-universite.fr/hal-02143873 Submitted on 29 May 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License fmicb-10-01024 May 9, 2019 Time: 14:44 # 1 ORIGINAL RESEARCH published: 10 May 2019 doi: 10.3389/fmicb.2019.01024 Impact of Leptospermone, a Natural b-Triketone Herbicide, on the Fungal Composition and Diversity of Two Arable Soils Clarisse Mallet1*, Sana Romdhane2,3, Camille Loiseau1, Jérémie Béguet2, Fabrice Martin-Laurent2, Christophe Calvayrac3,4 and Lise Barthelmebs3,4 1 Laboratoire Microorganismes : Génome et Environnement, CNRS, Université Clermont Auvergne, Clermont-Ferrand, France, 2 AgroSup Dijon, INRA UMR1347 Agroécologie, Université de Bourgogne, Université Bourgogne Franche-Comté, Dijon, France, 3 Biocapteurs-Analyses-Environnement, Université de Perpignan Via Domitia, Perpignan, France, 4 Laboratoire de Biodiversité et Biotechnologies Microbiennes, USR 3579 Sorbonne Universités (UPMC) Paris 6 et CNRS Observatoire Océanologique, Banyuls-sur-Mer, France Impact of leptospermone, a b-triketone bioherbicide, was investigated on the fungal community which supports important soil ecological functions such as decomposition of organic matter and nutrients recycling. This study was done in a microcosm experiment using two French soils, Perpignan (P) and Saint-Jean-de-Fos (SJF), differing in their physicochemical properties and history treatment with synthetic b-triketones. Soil microcosms were treated with leptospermone at recommended dose and incubated Edited by: Prayad Pokethitiyook, under controlled conditions for 45 days. Untreated microcosms were used as control. Mahidol University, Thailand Illumina MiSeq sequencing of the internal transcribed spacer region of the fungal rRNA Reviewed by: revealed significant changes in fungal community structure and diversity in both soils. Mariusz Cycon,´ Medical University of Silesia, Poland Xylariales, Hypocreales, Pleosporales and Capnodiales (Ascomycota phyla) fungi and Anna Poli, those belonging to Sebacinales, Cantharellales, Agaricales, Polyporales, Filobasidiales University of Turin, Italy and Tremellales orders (Basidiomycota phyla) were well represented in treated soil *Correspondence: microcosms compared to control. Nevertheless, while for the treated SJF a complete Clarisse Mallet [email protected] recovery of the fungal community was observed at the end of the experiment, this was not the case for the P treated soil, although no more bioherbicide remained. Indeed, the Specialty section: relative abundance of most of the saprophytic fungi were lower in treated soil compared This article was submitted to Microbiotechnology, Ecotoxicology to control microcosms whereas fungi from parasitic fungi included in Spizellomycetales and Bioremediation, and Pezizales orders increased. To the best of our knowledge, this is the only study a section of the journal Frontiers in Microbiology assessing the effect of the bioherbicide leptospermone on the composition and diversity Received: 14 December 2018 of the fungal community in soil. This study showed that leptospermone has an impact on Accepted: 24 April 2019 a- and b-diversity of the fungal community. It underlines the possible interest of microbial Published: 10 May 2019 endpoints for environmental risk assessment of biopesticide. Citation: Mallet C, Romdhane S, Keywords: fungal community, microbial ecotoxicology, bioherbicide, leptospermone, soil Loiseau C, Béguet J, Martin-Laurent F, Calvayrac C and Barthelmebs L (2019) Impact INTRODUCTION of Leptospermone, a Natural β-Triketone Herbicide, on the Fungal Composition and Diversity of Two The use of biopesticides, defined as natural active compounds, is viewed as a safe alternative Arable Soils. to agrochemicals for crop protection as they are considered to be less harmful and Front. Microbiol. 10:1024. environmental-friendly compared to synthetic pesticides (Dayan et al., 2007, 2011; Seiber et al., doi: 10.3389/fmicb.2019.01024 2014). Nowadays, only thirteen bioherbicides are commercially available (Cordeau et al., 2016). Frontiers in Microbiology| www.frontiersin.org 1 May 2019| Volume 10| Article 1024 fmicb-10-01024 May 9, 2019 Time: 14:44 # 2 Mallet et al. Impact of Leptospermone on Fungi Among compound of interest, leptospermone [2,2,4,4- TABLE 1 | Physico-chemical characteristics of the two soils (P and SJF) used tetramethyl-6-(3-methyl-1-oxobutyl)-1,3,5-cyclohexanetrione], for the experiment. an allelopathic compound isolated from bottlebrush plant Soil P Soil SJF Soil (Callistemon citrinus) was used as pre-and post-emergence characteristics herbicide to control broad leaf and grass weeds at a rate of 3 L ha−1 (Dayan et al., 2011). Belonging to b-triketone Clay 13.9% 25.8% family, leptospermone inhibits the 4-hydroxyphenylpyruvate Silt 60.5% 27.3% dioxygenase (HPPD), a key enzyme in plant carotenoid Sand 25.6% 46.9% biosynthesis, (Rocaboy-Faquet et al., 2014) leading to Soil humidity, 20% 15% Organic matter 1.7% 1.5% photosynthetic chlorophyll destruction of plant (Lee et al., Organic carbon 0.98% 0.9% 2008). However, HPPDs are not specific for plant and are found Cation 15.5 meq 100 g−1 10.4 meq 100 g−1 in prokaryotes and fungi, including those living in soil (Keon exchange and Hargreaves, 1998). Soil microorganisms which are known capacity (CEC) to accomplish numerous functions supporting soil ecosystemic Ca2C/CEC 214% 98% services are key drivers to be protected (EFSA, 2017). As pH in water 8.1. 7.62 recently underlined by Amichot et al.(2018) the side effect of History Experimental field Neither cultivated biopesticides has to be addressed, particularly assessing their site having a nor treated with environmental fate and impact on soil microorganisms (Gopal b-triketone history pesticides for the et al., 2007; Gupta et al., 2013; Singh et al., 2015a,b; Romdhane treatment last 5 years et al., 2016), and to the best of our knowledge no studies have been performed to estimate the effect of biopesticides on dose (D1, 5 mg g−1) or not (D0, control). For each soil, three fungal community (Thomson et al., 2015). Fungi are known randomly chosen microcosms were sacrificed by sampling date to play fundamental ecological roles in natural and managed and treatment (n = 12 per sampling date). Soil samples were agricultural soils (Al-Sadi et al., 2015; Tardy et al., 2015). As it then subdivided in different aliquots for dissipation studies and was previously observed, application of pesticides, even at the molecular analysis. recommended field dose, can induce a reduction in the overall fungal community, that could impacted the ecosystem services Fate of Leptospermone in the Soil in which fungi are involved (Sebiomo et al., 2011; Schlatter et al., 2018). On the other hand, pesticides can be used as carbon source Microcosms by some fungi known to possess biodegradation abilities (Ikehata Kinetics of dissipation and adsorption observed in P and SJF et al., 2004; Tortella et al., 2005; Coppola et al., 2011; Panelli et al., soils have already been reported in Romdhane et al.(2016). 2017; Góngora-Echeverría et al., 2018). Briefly, leptospermone dissipation was measured during the time Within this context, this study assessed for the first time, course of the incubation. Soil extracts were prepared from 10 g the impact of the bioherbicide leptospermone on the structure of each soil, and analyzed by HPLC/UV (Romdhane et al., 2016). and diversity of fungal community inhabiting two soil types. Calibration curves prepared with spiked blank soil samples, were We tested the effect of leptospermone on the diversity and used to determine the leptospermone in soil extracts, with a −1 composition of the fungal communities during the experimental quantification limit of 0.2 mg L . time and in a same manner in the two different soils. Adaptation of the batch equilibrium method was applied This goal was reached by high throughput deep sequencing to determine adsorption isotherms of leptospermone to both [Illumina MiSeq-based amplicon sequencing of ribosomal soils, using soil samples spiked with a range of leptospermone −1 internal transcribed spacer 2 (ITS2) region]. The richness of each solutions (1 to 40 mg L )(Wilson and Chester, 1992; OECD, sample (a-diversity) and the diversity in composition among 2000; Romdhane et al., 2016). After 3 h of agitation with samples (b-diversity) were assessed over time. 1 g of soil sample, remaining
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