TY - JOUR
T1 - A trait-based ecological perspective on the soil microbial antibiotic-related genetic machinery
AU - Dulya, Olesya
AU - Mikryukov, Vladimir
AU - Shchepkin, Daniil V.
AU - Pent, Mari
AU - Tamm, Heidi
AU - Guazzini, Massimo
AU - Panagos, Panos
AU - Jones, Arwyn
AU - Orgiazzi, Alberto
AU - Marroni, Fabio
AU - Bahram, Mohammad
AU - Tedersoo, Leho
PY - 2024/8
Y1 - 2024/8
N2 - Antibiotic resistance crisis dictates the need for resistance monitoring and the search for new antibiotics. The development of monitoring protocols is hindered by the great diversity of resistance factors, while the “streetlight effect” denies the possibility of discovering novel drugs based on existing databases. In this study, we address these challenges using high-throughput environmental screening viewed from a trait-based ecological perspective. Through an in-depth analysis of the metagenomes of 658 topsoil samples spanning Europe, we explored the distribution of 241 prokaryotic and fungal genes responsible for producing metabolites with antibiotic properties and 485 antibiotic resistance genes. We analyzed the diversity of these gene collections at different levels and modeled the distribution of each gene across environmental gradients. Our analyses revealed several nonparallel distribution patterns of the genes encoding sequential steps of enzymatic pathways synthesizing large antibiotic groups, pointing to gaps in existing databases and suggesting potential for discovering new analogues of known antibiotics. We show that agricultural activity caused a continental-scale homogenization of microbial antibiotic-related machinery, emphasizing the importance of maintaining indigenous ecosystems within the landscape mosaic. Based on the relationships between the proportion of the genes in the metagenomes with the main predictors (soil pH, land cover type, climate temperature and humidity), we illustrate how the properties of chemical structures dictate the distribution of the genes responsible for their synthesis across environments. With this understanding, we propose general principles to facilitate the discovery of antibiotics, including principally new ones, establish abundance baselines for antibiotic resistance genes, and predict their dissemination.
AB - Antibiotic resistance crisis dictates the need for resistance monitoring and the search for new antibiotics. The development of monitoring protocols is hindered by the great diversity of resistance factors, while the “streetlight effect” denies the possibility of discovering novel drugs based on existing databases. In this study, we address these challenges using high-throughput environmental screening viewed from a trait-based ecological perspective. Through an in-depth analysis of the metagenomes of 658 topsoil samples spanning Europe, we explored the distribution of 241 prokaryotic and fungal genes responsible for producing metabolites with antibiotic properties and 485 antibiotic resistance genes. We analyzed the diversity of these gene collections at different levels and modeled the distribution of each gene across environmental gradients. Our analyses revealed several nonparallel distribution patterns of the genes encoding sequential steps of enzymatic pathways synthesizing large antibiotic groups, pointing to gaps in existing databases and suggesting potential for discovering new analogues of known antibiotics. We show that agricultural activity caused a continental-scale homogenization of microbial antibiotic-related machinery, emphasizing the importance of maintaining indigenous ecosystems within the landscape mosaic. Based on the relationships between the proportion of the genes in the metagenomes with the main predictors (soil pH, land cover type, climate temperature and humidity), we illustrate how the properties of chemical structures dictate the distribution of the genes responsible for their synthesis across environments. With this understanding, we propose general principles to facilitate the discovery of antibiotics, including principally new ones, establish abundance baselines for antibiotic resistance genes, and predict their dissemination.
KW - Antibiotic biosynthesis
KW - Antibiotic resistance
KW - Metagenome
KW - Secondary metabolites
KW - Soil
KW - Trait
UR - http://www.scopus.com/inward/record.url?scp=85200104334&partnerID=8YFLogxK
U2 - 10.1016/j.envint.2024.108917
DO - 10.1016/j.envint.2024.108917
M3 - Journal article
C2 - 39089094
AN - SCOPUS:85200104334
SN - 0160-4120
VL - 190
JO - Environment International
JF - Environment International
M1 - 108917
ER -