The Role of Agriculture in the Dissemination of Class 1 Integrons, Antimicrobial Resistance, and Diversity of Their Gene Cassettes in Southern China

Abstract

Integrons are hot spots for acquiring gene cassettes from the environment and play a major role in the bacterial evolution and dissemination of antimicrobial resistance (AMR), thus posing a serious threat. There are currently studies on integrons and antibiotic resistance genes; however, the presence and association of integrons in different agricultural crops and their subsequent dissemination and role in AMR have not been reported previously. This study examines the abundance of integrons, their gene cassette diversity in various crop soils, and their role in the dissemination of AMR in the southern region of China. Samples from different agri-crop soil, such as rice (R.S), sugarcane (S.S), citrus (C.S), banana (B.S), agricultural runoff (the point where the runoff of all sites meet (R.O)), and wild (non-agricultural) soil (W.S), were collected. Quantitative PCR was used to determine the abundance of integrons, and clone libraries were constructed to examine the gene cassette arrays. All the tested samples were found positive for Class-I (CL1) integrons and revealed a higher concentration and higher relative abundance of R.S than the others, with the least found at the W.S site. The W.S CL1 cassette arrays were found empty, and no putative conserved domains were found. The R.O was found to contain a high number of gene cassettes with various functions, while the smallest number of gene cassettes was found in the S.S among the crop soils. Most of the gene cassettes presented by the R.O were primarily shared with other sites, and the antibiotic-resistant genes were consistently observed to be dominant. The constructed clone libraries represented a diverse gene cassette array with 16% novel gene cassettes that play a vital role in pathogenesis, transportation, biosynthesis, and AMR. Most resistance-related gene cassettes were associated with the genes encoding resistance to quaternary ammonium compound (QAC) and aminoglycosides. This study highlights the significant differences in the abundance of integrons among various agricultural soils and offers deep insight into the pools of gene cassettes that play a key role in the dissemination of integrons and AMR.

Biochar and Manure Applications Differentially Altered the Class 1 Integrons, Antimicrobial Resistance, and Gene Cassettes Diversity in Paddy Soils

“…Gene cassettes are enormous reservoirs of genetic diversity and play a major role in the evolution of bacteria to specific conditions ( Gillings, 2014 ). Our clone library analysis of gene cassettes showed that most of the gene cassettes encoding polypeptides either had no homology in the database or had so with hypothetical proteins and were novel, which was in line with the previous studies conducted in the environmental settings of integron gene cassettes ( Elsaied et al, 2007 ; Koenig et al, 2009 ; An et al, 2018 ; Ali et al, 2020a ).…”

“…However, according to certain studies, the effect of biochar ARGs depends on the type of biochar and manure utilized (Cui et al, 2017). The abundance of integrons and accompanying antimicrobial resistance in paddy fields in a typical agricultural ecological setting of Guangxi was substantially higher than in sugarcane fields, according to our earlier study (Ali et al, 2020a). The paddy fields have different forms of anthropogenic inputs resulting in the high abundance of integrons and their subsequent gene cassettes array.…”

“…We also found different classes of ARGs in M and C treatments, separately; however, the most prevalent were the aminoglycosides across all treatments. They harbored nucleotide transferase enzyme, resisted different types of aminoglycosides, and had a resemblance with the kanamycin resistance gene ( Martí et al, 2019 ; Ali et al, 2020a ).…”

“…Antibiotic resistance evolves as a result of mutations in the genome, with horizontal gene transfer (HGT) being a well-known phenomenon in this context ( Zhu et al, 2017 ; Lima et al, 2020 ). HGT facilitates bacterial adaptive behavior and rapid evolution and promotes antimicrobial resistance genes (ARGs) across bacteria species in the environment ( Martínez, 2008 ; Zhu et al, 2017 ; Ali et al, 2020a ). Mobile genetic elements (MGEs) mediate the HGT, which could enhance the lateral gene flow among the clinical isolates ( Stecher et al, 2012 ; Chen et al, 2016 ; An et al, 2018 ; Khan et al, 2022 ).…”

“…The initial component is at the 5′ conserved region (5′CS), which includes an integrase (intI) gene, an attI recombination site, and a promoter (Pc) region. This platform acquires GCs and expresses them in a row if the gene cassette lacks the open reading frames (ORF; Peterson and Kaur, 2018 ; Ali et al, 2020a ; Ghaly et al, 2020 ).…”