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

• Published in: Frontiers in microbiology 2021-03, Vol.12, p.643087
• Main Authors: Billet, Loren, Pesce, Stéphane, Rouard, Nadine, Spor, Aymé, Paris, Laurianne, Leremboure, Martin, Mounier, Arnaud, Besse-Hoggan, Pascale, Martin-Laurent, Fabrice, Devers-Lamrani, Marion
• Format: Article
• Language: English
• Subjects: antibiotic biodegradation; bacterial community invasion; Life Sciences; microbial ecotoxicology; Microbiology; soil; sulfonamide
• ISSN: 1664-302X; 1664-302X
• DOI: 10.3389/fmicb.2021.643087

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 sp. C448 was inoculated in four different soil types with and without added sulfamethazine and/or swine manure. After 1 month of incubation, sp. (and its antibiotrophic gene ) 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 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 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 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.