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Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448
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 adva...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2021
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8032547/ https://www.ncbi.nlm.nih.gov/pubmed/33841365 http://dx.doi.org/10.3389/fmicb.2021.643087 |
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author | Billet, Loren Pesce, Stéphane Rouard, Nadine Spor, Aymé Paris, Laurianne Leremboure, Martin Mounier, Arnaud Besse-Hoggan, Pascale Martin-Laurent, Fabrice Devers-Lamrani, Marion |
author_facet | Billet, Loren Pesce, Stéphane Rouard, Nadine Spor, Aymé Paris, Laurianne Leremboure, Martin Mounier, Arnaud Besse-Hoggan, Pascale Martin-Laurent, Fabrice Devers-Lamrani, Marion |
author_sort | Billet, Loren |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-8032547 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-80325472021-04-09 Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448 Billet, Loren Pesce, Stéphane Rouard, Nadine Spor, Aymé Paris, Laurianne Leremboure, Martin Mounier, Arnaud Besse-Hoggan, Pascale Martin-Laurent, Fabrice Devers-Lamrani, Marion Front Microbiol Microbiology 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. Frontiers Media S.A. 2021-03-26 /pmc/articles/PMC8032547/ /pubmed/33841365 http://dx.doi.org/10.3389/fmicb.2021.643087 Text en Copyright © 2021 Billet, Pesce, Rouard, Spor, Paris, Leremboure, Mounier, Besse-Hoggan, Martin-Laurent and Devers-Lamrani. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Billet, Loren Pesce, Stéphane Rouard, Nadine Spor, Aymé Paris, Laurianne Leremboure, Martin Mounier, Arnaud Besse-Hoggan, Pascale Martin-Laurent, Fabrice Devers-Lamrani, Marion Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448 |
title | Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448 |
title_full | Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448 |
title_fullStr | Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448 |
title_full_unstemmed | Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448 |
title_short | Antibiotrophy: Key Function for Antibiotic-Resistant Bacteria to Colonize Soils—Case of Sulfamethazine-Degrading Microbacterium sp. C448 |
title_sort | antibiotrophy: key function for antibiotic-resistant bacteria to colonize soils—case of sulfamethazine-degrading microbacterium sp. c448 |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8032547/ https://www.ncbi.nlm.nih.gov/pubmed/33841365 http://dx.doi.org/10.3389/fmicb.2021.643087 |
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