Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448

Abstract

Chronic and repeated exposure of environmental bacterial communities to anthropogenic antibiotics have recently driven some antibiotic-resistant bacteria to acquire catabolic functions, enabling them to use antibiotics as nutritive sources (antibiotrophy). Antibiotrophy might confer a selective advantage facilitating the implantation and dispersion of antibiotrophs in contaminated environments. A microcosm experiment was conducted to test this hypothesis in an agroecosystem context. The sulfonamide-degrading and resistant bacterium Microbacterium sp. C448 was inoculated in four different soil types with and without added sulfamethazine and/or swine manure. After 1 month of incubation, Microbacterium sp. (and its antibiotrophic gene sadA) was detected only in the sulfamethazine-treated soils, suggesting a low competitiveness of the strain without antibiotic selection pressure. In the absence of manure and despite the presence of Microbacterium sp. C448, only one of the four sulfamethazine-treated soils exhibited mineralization capacities, which were low (inferior to 5.5 ± 0.3%). By contrast, manure addition significantly enhanced sulfamethazine mineralization in all the soil types (at least double, comprised between 5.6 ± 0.7% and 19.5 ± 1.2%). These results, which confirm that the presence of functional genes does not necessarily ensure functionality, suggest that sulfamethazine does not necessarily confer a selective advantage on the degrading strain as a nutritional source. 16S rDNA sequencing analyses strongly suggest that sulfamethazine released trophic niches by biocidal action. Accordingly, manure-originating bacteria and/or Microbacterium sp. C448 could gain access to low-competition or competition-free ecological niches. However, simultaneous inputs of manure and of the strain could induce competition detrimental for Microbacterium sp. C448, forcing it to use sulfamethazine as a nutritional source. Altogether, these results suggest that the antibiotrophic strain studied can modulate its sulfamethazine-degrading function depending on microbial competition and resource accessibility, to become established in an agricultural soil. Most importantly, this work highlights an increased dispersal potential of antibiotrophs in antibiotic-polluted environments, as antibiotics can not only release existing trophic niches but also form new ones.

Experimental Evidence for Manure-Borne Bacteria Invasion in Soil During a Coalescent Event: Influence of the Antibiotic Sulfamethazine

“…Finally, the impact of the antibiotic SMZ on the structure of autochthonous soil bacterial communities was relatively low as it was significant in only one of the four soils (soil A). Previous results obtained from the same microcosms may explain this fact [30]. After 1 month of incubation, the bioavailable fraction of SMZ in the SMZ-treated soils represented a low level of exposure for the community.…”

“…DNA was extracted from subsamples of 250 mg of soil for each microcosm using the DNeasy PowerSoil-htp 96-well DNA isolation kit (Qiagen, France) following the manufacturer's instructions and stored at −20°C. As previously described by Billet et al (2021), the V3-V4 hypervariable region of the bacterial 16S rRNA gene was amplified using a two-step PCR and sequenced on MiSeq (Illumina, 2 × 250 bp) and a Jupyter Notebook developed in-house was used to analyze the sequence data [30]. Briefly, sequences were assembled using PEAR [33] with default settings.…”

“…Consequently, contamination of soil with antibiotics originating from manure amendment is likely to promote the invading potential of antibiotic-resistant manure-borne bacteria in soils. In that sense, antibiotics could increase the invading potential of isolated antibiotic-resistant strains in soil [29,30] and manure amendment can result in an increase of the diversity of antibiotic-resistant bacteria in soil [19].…”

Construction and Characterization of an Intergeneric Fusant That Degrades the Fungicides Chlorothalonil and Carbendazim

“…Microbacterium sp. WHC1 can effectively remove Ciprofloxacin (CIP) for biological repair ( Billet et al, 2021 ; Hu et al, 2021 ; Sodhi et al, 2021 ; Wongbunmak et al, 2021 ).…”

Experimental Evidence for Manure-Borne Bacteria Invasion in Soil During a Coalescent Event: Influence of the Antibiotic Sulfamethazine

“…The four soils, named A,B,C and D selected for their different textures as described by Billet et al, (2021), were sampled from the upper 20 cm of different agricultural elds the Bourgogne-Franche-Comté region of France in November 2018. They originated respectively from an agricultural eld frequently ooded by the nearby Saône River, the same plot but at a higher altitude, the experimental farm of Epoisses, and a eld near a hog nursery that had received manure 6 months before the sampling.…”