Land application of beef cattle manure facilitates the transmission of antibiotic resistance genes from soil to lettuce

Abstract

The land application of livestock manure can have significant effects on the emergence and proliferation of antibiotic resistance genes (ARGs) and antibiotic residues in the soil–plant ecosystem. While previous studies have documented the effects of manure application on ARGs in either soil or plant compartments, research addressing its impact on ARGs concurrently in both soil and plants remains relatively limited. This study aims to assess the occurrence of ARGs in and on lettuce cultivated in soil with beef cattle manure application. Results showed that seven ARGs (bla_TEM, erm(B), erm(F), tet(M), tet(O), tet(Q), and tet(X)) and one class 1 integron–integrase gene (intI1) were quantified in both soil and lettuce compartments following manure application. The relative abundance of manure-borne tet(M), tet(Q), and tet(X) was significantly elevated in surface soils (Kruskal–Wallis tests, p < 0.05). Notably, tet genes increased by 1–3 orders of magnitude within the lettuce endosphere and roots, revealing a potential transmission from soil to lettuce. In contrast, the relative abundance of bla_TEM, erm(B), and erm(F) increased only in the episphere and root but not within the endosphere of lettuce. Additionally, concentrations of tylosin in surface soil showed positive correlations with tet genes, suggesting their potential roles in facilitating the ARG proliferation in the soil–plant ecosystem. In summary, this study demonstrates that manure application promoted the transmission of manure-borne ARGs from soil to lettuce, highlighting a potential pathway for human exposure to antimicrobial resistance through the food chain. This finding underscores the need for the development of manure management practices to mitigate ARG spread in agriculture.