Co‐occurrence of antibiotic, biocide, and heavy metal resistance genes in bacteria from metal and radionuclide contaminated soils at the Savannah River Site

Abstract

Contaminants such as heavy metals may contribute to the dissemination of antimicrobial resistance (AMR) by enriching resistance gene determinants via co-selection mechanisms. In the present study, a survey was performed on soils collected from four areas at the Savannah River Site (SRS), South Carolina, USA, with varying contaminant profiles: relatively pristine (Upper Three Runs), heavy metals (Ash Basins), radionuclides (Pond B) and heavy metal and radionuclides (Tim's Branch). Using 16S rRNA gene amplicon sequencing, we explored the structure and diversity of soil bacterial communities. Sites with legacies of metal and/or radionuclide contamination displayed significantly lower bacterial diversity compared to the reference site. Metagenomic analysis indicated that multidrug and vancomycin antibiotic resistance genes (ARGs) and metal resistance genes (MRGs) including those associated with copper, arsenic, iron, nickel and zinc were prominent in all soils including the reference site. However, significant differences were found in the relative abundance and diversity of certain ARGs and MRGs in soils with metal/radionuclide contaminated soils compared to the reference site. Co-occurrence patterns revealed significant ARG/MRG subtypes in predominant soil taxa including Acidobacteriaceae, Bradyrhizobium, Mycobacterium, Streptomyces, Verrumicrobium, Actinomadura and Solirubacterales. Overall, the study emphasizes the potential risk of human activities on the dissemination of AMR in the environment.

Is Long-Term Heavy Metal Exposure Driving Carriage of Antibiotic Resistance in Environmental Opportunistic Pathogens: A Comprehensive Phenomic and Genomic Assessment Using Serratia sp. SRS-8-S-2018

“…SRS-8-S-2018 indicates that the strain has acquired resistance to multiple antibiotics, most likely exacerbated by exposure to Hg, U and possibly other heavy metal contamination in the SRS soils. These findings are in line with previous body of information on SRS soils, which unequivocally show that the legacy contaminated SRS soils serve as a repository for acquisition of both metal and antibiotic resistances ( Stepanauskas et al, 2006 ; Wright et al, 2006 ; Thomas et al, 2020 ). However, this study is focused on Serratia spp., which are opportunistic pathogens and brings out the necessity for further focused studies on this aspect rather than a more generalized assessment of the proliferation and abundance of MRGs and ARGs within the SRS soil habitat, as has been the case with most previous studies.…”

“…Our recent studies suggest that the metalliferous SRS soils may be serving as a reservoir for the recruitment and proliferation of metal and antimicrobial resistances in the native microbial communities ( Agarwal et al, 2019 , 2020a , 2020b ; Gendy et al, 2020a , b ; Pathak et al, 2020 ), thus presenting risks to the ecological processes and public health. Overall, this study further builds upon evidence to show that the SRS contaminated soils inherently harbor higher antibiotic resistance, relative to the reference soils, and thus driving antimicrobial resistance to the native microbiota, including several known pathogens (e.g., Burkholderia , Ralstonia , Massilia , Acinetobacter , and Pseudomonas ( Stepanauskas et al, 2006 ; Wright et al, 2006 ; Thomas et al, 2020 ). To assess if carriage of metal resistant genes (MRGs), and antibiotic resistant genes (ARGS) is a rampantly widespread trait, especially within opportunistic bacteria native to the SRS soils, this study was conducted on soils collected from a different site (101), relative to that reported by our group recently ( Pathak et al, 2020 ).…”

“…Despite this advantage of microbially based heavy metal bioremediation, studies have also unequivocally shown that bacteria can acquire antibiotic resistance when exposed to long-term contamination, especially with Hg and U ( Benyehuda et al, 2003 ), including our previous work ( Agarwal et al, 2019 , 2020a , b ; Gendy et al, 2020a , b ; Pathak et al, 2020 ). This builds upon significant evidence that exists on the SRS soils which unequivocally shows higher levels of antibiotic resistance in contaminated SRS soils relative to reference soils ( Stepanauskas et al, 2006 ; Wright et al, 2006 ; Thomas et al, 2020 ). Furthermore, both, empirical and anecdotal evidence from SRS soils strongly suggest recruitment of antibiotic resistances in many human pathogens that are native to these soils [e.g., Burkholderia , Ralstonia , Massilia , Acinetobacter , and Pseudomonas ( Stepanauskas et al, 2006 )].…”

High‐throughput molecular analyses of microbiomes as a tool to monitor the wellbeing of aquatic environments

“…The prevalence and dissemination of antimicrobial resistance (AMR) is an increasingly serious threat to global public health (WHO, 2015;Qiao et al, 2018;Thomas et al, 2020), that has turned into an emergency in lowincome countries (Bastaraud et al, 2020). Consequently, a significant reduction in the effectiveness of antibiotics and other antimicrobial agents (antifungals, antivirals, antimalarials, and anthelmintics) threatens our ability to treat common infectious diseases, resulting in prolonged illness, disability, and death (Wright, 2010;Almakki et al, 2019).…”

Improved microbial community characterization of 16S rRNA via metagenome hybridization capture enrichment

“…Thus, expensive deep sequencing is unnecessary for 16S-cap libraries because a few thousand reads provide the same number of 16S rRNA sequences as millions of shotgun reads. By trading modest additional library preparation costs for reduced sequencing costs ( Supplementary Tables 3-5), 16S cap is economical and opens up the possibility of adding deep taxonomic sampling to studies that are capturing other genes of interests (e.g., antibiotic resistance genes (Guitor et al, 2019;Oladeinde et al, 2019;Thomas et al, 2020). In comparison to amplicon libraries, the 16S-cap assay will be more expensive, however, it provides superior microbial community resolution, increased accuracy of relative abundance, and greater flexiblity in terms of sequencer and kit choice.…”