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Metagenomic profiling of antibiotic resistance genes in Red Sea brine pools

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Abstract

Antibiotic resistance (AR) is an alarming global health concern, causing an annual death rate of more than 35,000 deaths in the US. AR is a natural phenomenon, reported in several pristine environments. In this study, we report AR in pristine Red Sea deep brine pools. Antimicrobial resistance genes (ARGs) were detected for several drug classes with tetracycline and macrolide resistance being the most abundant. As expected, ARGs abundance increased in accordance with the level of human impact with pristine Red Sea samples having the lowest mean ARG level followed by estuary samples, while activated sludge samples showed a significantly higher ARG level. ARG hierarchical clustering grouped drug classes for which resistance was detected in Atlantis II Deep brine pool independent of the rest of the samples. ARG abundance was significantly lower in the Discovery Deep brine pool. A correlation between integrons and ARGs abundance in brine pristine samples could be detected, while insertion sequences and plasmids showed a correlation with ARGs abundance in human-impacted samples not seen in brine pristine samples. This suggests different roles of distinct mobile genetic elements (MGEs) in ARG distribution in pristine versus human-impacted sites. Additionally, we showed the presence of mobile antibiotic resistance genes in the Atlantis II brine pool as evidenced by the co-existence of integrases and plasmid replication proteins on the same contigs harboring predicted multidrug-resistant efflux pumps. This study addresses the role of non-pathogenic environmental bacteria as a silent reservoir for ARGs, and the possible horizontal gene transfer mechanism mediating ARG acquisition.

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Availability of data and materials

The datasets used and/or analyzed during the current study are available from SRA (https://www.ncbi.nlm.nih.gov/sra) and IMG (https://img.jgi.doe.gov) under the accession numbers available in Table S1.

Abbreviations

AR:

Antibiotic resistance

ARG:

Antibiotic resistance gene

AS:

Activated sludge

ATIID:

Atlantis II deep

CARD:

Comprehensive antibiotic resistance database

DD:

Discovery deep

IS:

Insertion sequence

KD:

Kebrit deep

MGE:

Mobile genetic element

RGI:

Resistance gene identifier

WWTP:

Wastewater treatment plant

References

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Acknowledgements

We thank Nahu Dimitri, Christiane Martell Rodriguez, Jennifer Beniquez Martir, Arve Cooper and Tiana Junor for the valuable discussions on extreme environments literature.

Funding

The work was partially funded by an American University in Cairo Faculty (Research) Support Grant to RS. The funding body did not have a role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

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Authors

Contributions

AHAE designed and performed the work, analyzed and presented the data, and wrote the initial manuscript draft. EB analyzed data, collected literature and wrote the manuscript. RS designed the research, directed the data analysis and wrote the manuscript.

Corresponding authors

Correspondence to Ali H. A. Elbehery or Rania Siam.

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The authors declare that they have no competing interests.

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Communicated by Yusuf Akhter.

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Elbehery, A.H.A., Beason, E. & Siam, R. Metagenomic profiling of antibiotic resistance genes in Red Sea brine pools. Arch Microbiol 205, 195 (2023). https://doi.org/10.1007/s00203-023-03531-x

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  • DOI: https://doi.org/10.1007/s00203-023-03531-x

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