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

Authors: THOMAS, JESSE - CENTERS FOR DISEASE CONTROL AND PREVENTION (CDC) - UNITED STATES; Oladeinde, Adelumola - Ade; KIERANT, TROY - UNIVERSITY OF GEORGIA; FINGER, JOHN - AUBURN UNIVERSITY; VASQUEZ, NATALIA - UNIVERSITY OF GEORGIA; CARTEE, JOHN - UNIVERSITY OF GEORGIA; BEASLEY, JAMES - UNIVERSITY OF GEORGIA; SEAMAN, JOHN - UNIVERSITY OF GEORGIA; MCARTHUR, VAUN - UNIVERSITY OF GEORGIA; RHODES, OLIN - UNIVERSITY OF GEORGIA; GLENN, TRAVIS - UNIVERSITY OF GEORGIA

Submitted to: Microbial Biotechnology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/1/2020
Publication Date: 5/3/2020
Citation: Thomas, J., Oladeinde, A.A., Kierant, T., Finger, J., Vasquez, N., Cartee, J., Beasley, J., Seaman, J., Mcarthur, V., Rhodes, O., Glenn, T. 2020. Co-occurrence of antibiotic, biocide, and heavy metal resistance genes in bacteria from metal and radionuclide contaminated soils at the Savannah River Site. Microbial Biotechnology. https://doi.org/10.1111/1751-7915.13578.
DOI: https://doi.org/10.1111/1751-7915.13578

Interpretive Summary: If we are to stop the epidemic increase in bacteria with resistance to antibiotics of public health concern, it is critical we understand how and why a susceptible bacteria may acquire and maintain resistance to antibiotics. Exposure of bacteria to metals has been suggested as a predisposing factor for acquisition of antibiotic resistance. In this study, we examined the Savannah River Site (SRS) soils for bacterial communities carrying metal and antibiotic resistance genes. The SRS served as the Department of Energy (DOE) production and refinement facility for nuclear materials from 1950 - 1980, therefore the soil has widespread contamination with heavy metals, metalloids, and radionuclides. We examined bacteria isolated from soil in multiple sites on SRS. Our results show that strong relationships exist between the microbial community in soils at the SRS, and the presence of chronic heavy metal and radionuclide contamination. We found that certain bacterial species are differentially affected by soil edaphic factors and heavy metal contamination, and that the presence of soil contamination is related to dissemination and maintenance of antibiotic and metal resistance.

Technical Abstract: Soil environments represent a significant reservoir of microbial diversity and antimicrobial resistance (AMR) genes. Contaminants such as heavy metals may contribute to the dissemination of 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 metal contaminated (Ash Basins), radionuclide contaminated (Pond B), and heavy metal with radionuclide contaminated (Tim’s Branch). We explored the relative abundance, diversity, and structure of soil bacterial communities using of 16S rRNA gene amplicon sequencing, and obtained 6,078,406 high quality (Q ' 20) sequences, revealing a core microbiome consisting of eight phyla shared among 95% of the sequences. Sites with records of metal/radionuclide contamination displayed significantly lower bacterial diversity compared to the reference. Metal concentrations and carbon to nitrogen (C:N) ratio were the most important factors determining the microbial community structure. Metagenomic analysis indicated that among antibiotic resistance genes (ARGs), multidrug and vancomycin resistance genes were most prominent in all soil samples including those from the pristine site. Metal resistance genes (MRGs) were dominated by those associated with copper, arsenic, iron, nickel, zinc, molybdenum resistance, and multi-metal resistance. Significant differences were found in the relative abundance and diversity of antibiotic, biocide, and metal resistance genes on soils with both metals and radionuclide contamination compared to the reference site. Co-occurrence patterns revealed significant ARG and MRG subtypes in predominant soil taxa including Acidobacteriaceae, Bradyrhizobium, Mycobacterium, Streptomyces, Verrumicrobium, Actinomadura, and Solirubacterales. Notably, these findings will help to understand the selective pressures human activities may exert on the resistome in contaminated environments, but also illuminate patterns of intrinsic antimicrobial resistance in those unperturbed.