ANTIBIOTOX: Fate of antibiotics and associated resistance genes in agroecosystems: ecotoxicological risk for functional microbial communities of receiving river systems

Coordinator:  Fabrice Martin-Laurent (INRAE – UMR Agroécologie, Dijon)

Partner PIs:

• Fabrice Martin-Laurent & Marion Devers (INRAE – UMR Agroécologie, Dijon)
• Stéphane Pesce & Chloé Bonnineau (INRAE – UR RiverLy, Lyon)
• Soizic Morin (INRAE – UR EABX, Bordeaux)
• Joan Artigas & Isabelle Batisson (Université Clermont-Auvergne – UMR LMGE, Clermont-Ferrand)
• Pascale Besse Hoggan (CNRS – UMR ICCF, Clermont-Ferrand)
• Cédric Malandain (Enoveo, Lyon)
• Ed Topp (Agriculture and Agri-Food Canada, London, Ontario, Canada)

General Objectives:

Pharmaceuticals including antibiotics, have a wide application range in human and veterinary medicines. It is noteworthy that veterinary antibiotics (VAs) used in livestock and poultry production for growth promotion, prophylaxis and treatment of illness are an important source of environmental contamination. Indeed, being designed for pharmacological stability, most VAs are recalcitrant to biodegradation after ingestion. They have been detected as contaminants in various environmental compartments where they cause human and environmental threats, notably with respect to the potential emergence and proliferation of antibiotic-resistant bacteria. To mitigate the risk represented by this emergence in agroecosystems, the French Ministry of Agriculture recently launched EcoAntibio, a national plan dedicated to reducing the risk of resistance to VAs. An important component of managing environmental risk caused by VAs is to understand exposure of soil and water resources to antibiotic residues and antibiotic-resistant bacteria and the antibiotic-resistance genes that they carry. One challenge is to gain knowledge on the fate of VAs in the ecosystem along the soil::water continuum, and on the collateral impact of VAs on environmental microorganisms responsible for crucially important ecosystem functions.

Fully 20% of the VAs used in food animal production in France are sulfonamides. In this context, the ANTIBIOTOX project aims at studying the environmental fate and impact of two VAs of the sulfonamides class of antibiotics, sulfamethazine (SMZ) and sulfamethoxazole (SMX). Specific objective of the ANTIBIOTOX project are to 1) elucidate processes involved in sulfonamide biodegradation by a bacterial strain (Microbacterium sp. C448), 2) study the impact of microbial biodegradation on the fate of SMZ and SMX and related metabolites in aquatic and terrestrial compartments of agroecosystems, 3) develop innovative tool (DNA microarray) to study the dissemination of sulfonamide resistant bacteria and genes from agricultural soil to adjacent water resources, 4) estimate the impact of sulfonamide residues and transformation products on the abundance of resistant microbes and on functional microbial communities in the aquatic receiving system, 5) disseminate the main outcomes of this research program to academic, policy, industry and other stakeholders using targeted communication tools, and contribute to the training of highly qualified staff.

This innovative project searches for new insights concerning the environmental impact of two sulfonamide antibiotics using integrated (from the gene to the ecosystem) and interdisciplinary approaches bringing together scientists from complementary disciplines (environmental microbiology, molecular biology (transcriptomics), biochemistry (proteomics), microbial ecotoxicology and analytical chemistry). It relies on established collaborations between the partners and on the access to long term experimental field experiments exposed to antibiotics and to Microbacterium sp. C448, the first known bacterial strain mineralizing SMZ (Associated partner; Agriculture Agri-Food Canada).

From an academic point of view, the expected results of ANTIBIOTOX will contribute to a better understanding of the fate and ecotoxicological impact of sulfonamides along the soil::water continuum with a strong focus on aquatic ecosystems. The obtained results will undeniably lead to improve knowledge on the genetic adaptation of microorganisms in response to antibiotic exposure and to the development of innovative tools for antibiotic environmental risk assessment with high-potential industrial applications.

Role of EMA Research Group:

Stéphane Pesce co-leads WP3 with Marion Devers: Potential dispersal of antibiotic resistances in agrosystems

Chloé Bonnineau co-leads WP4 with Cédric Malandain: Ecotoxicological effects of SMZ, SMX and metabolites on aquatic microbial communities

Related publications involving our EMA Research Group:

BILLET L, PESCE S, MARTIN-LAURENT F, DEVERS-LAMRANI M, 2023. Experimental evidence for manure-borne bacteria invasion in soil during a coalescent event: influence of the antibiotic sulfamethazine. Microb. Ecol. 85, 1463–1472. doi: 10.1007/s00248-022-02020-w. hal-04157280

BILLET L, PESCE S, ROUARD N, SPOR A, PARIS L, LEREMBOURE M, MOUNIER A, BESSE-HOGGAN P, MARTIN-LAURENT F, DEVERS-LAMRANI M, 2021. Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448. Front. Microbiol., 12:643087. doi: 10.3389/fmicb.2021.643087

KERGOAT L, BESSE-HOGGAN P, LEREMBOURE M, BEGUET J, DEVERS-LAMRANI M, MARTIN-LAURENT F, MASSON M, MORIN S, ROINAT A, PESCE S, BONNINEAU C, 2021. Environmental concentrations of sulfonamides can alter bacterial structure and induce diatom deformities in freshwater biofilm communities. Front. Microbiol. 12:643719

PESCE S, KERGOAT L, PARIS L, BILLET L, BESSE-HOGGAN P, BONNINEAU C, 2021. Contrasting effects of environmental concentrations of sulfonamides on microbial heterotrophic activities in freshwater sediment. Front. Microbiol. 12:753647. 

MARTIN-LAURENT F., TOPP E., BILLET L., BATISSON I., MALANDAIN C., BESSE-HOGGAN P., MORIN S., ARTIGAS J., BONNINEAU C., KERGOAT L., DEVERS-LAMRANI M., PESCE S., 2019.
Environmental risk assessment of antibiotics in agroecosystems: ecotoxicological effects on aquatic microbial communities and dissemination of antimicrobial resistances and antibiotic biodegradation potential along the soil-water continuum. Environmental Science and Pollution Research.