Research Article

Transcriptomics and methylomics study on the effect of iodine-containing drug FS-1 on Escherichia coli ATCC BAA-196

*Author for correspondence:

E-mail Address: laeda81@gmail.com

https://orcid.org/0000-0002-0397-7840

Department of Virology, Scientific Center for Anti-Infectious Drugs, Almaty, Kazakhstan

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Ardak B Jumagaziyeva

https://orcid.org/0000-0002-8610-7321

Department of Microbiology, Scientific Center for Anti-Infectious Drugs, Almaty, Kazakhstan

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Sergey V Shilov

https://orcid.org/0000-0001-9490-9300

Department of Virology, Scientific Center for Anti-Infectious Drugs, Almaty, Kazakhstan

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Tatyana V Kuznetsova

https://orcid.org/0000-0003-4186-3948

Department of Virology, Scientific Center for Anti-Infectious Drugs, Almaty, Kazakhstan

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Auyes N Myrzabayeva

https://orcid.org/0000-0003-1084-7427

Department of Microbiology, Scientific Center for Anti-Infectious Drugs, Almaty, Kazakhstan

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Zhanar A Iskakbayeva

https://orcid.org/0000-0001-7428-0074

Department of Microbiology, Scientific Center for Anti-Infectious Drugs, Almaty, Kazakhstan

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Aleksandr I Ilin

https://orcid.org/0000-0000-1952-8972

Department of Chemistry, Scientific Center for Anti-Infectious Drugs, Almaty, Kazakhstan

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Monique Joubert

Department of Biochemistry, Genetics & Microbiology, Centre for Bioinformatics & Computational Biology, University of Pretoria, Pretoria, South Africa

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Setshaba Taukobong

Department of Biochemistry, Genetics & Microbiology, Centre for Bioinformatics & Computational Biology, University of Pretoria, Pretoria, South Africa

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Oleg N Reva

**Author for correspondence:

E-mail Address: oleg.reva@up.ac.za

https://orcid.org/0000-0002-5459-2772

Department of Biochemistry, Genetics & Microbiology, Centre for Bioinformatics & Computational Biology, University of Pretoria, Pretoria, South Africa

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Published Online:1 Sep 2021

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Abstract

Aim: Promising results on application of iodine-containing nano-micelles, FS-1, against antibiotic-resistant Escherichia coli was demonstrated. Materials & methods: RNA sequencing for transcriptomics and the complete genome sequencing by SMRT PacBio were followed by genome assembly and methylomics. Results & conclusion: FS-1-treated E. coli showed an increased susceptibility to antibiotics ampicillin and gentamicin. Cultivation with FS-1 caused gene expression alterations toward anaerobic respiration, increased anabolism and inhibition of many nutrient uptake systems. Main targets of iodine-containing particles were cell membrane structures causing oxidative, osmotic and acidic stresses. Identification of methylated nucleotides showed an altered pattern in the FS-1-treated culture. Possible role of transcriptional and epigenetic modifications in the observed increase in susceptibility to gentamicin and ampicillin were discussed.

Lay abstract

New approaches of combatting drug-resistant infections are in demand as the development of new antibiotics is in a deep crisis. This study was set out to investigate molecular mechanisms of action of new iodine-containing nano-micelle drug FS-1, which potentially may improve the antibiotic therapy of drug-resistant infections. Iodine is one of the oldest antimicrobials and until now there were no reports on development of resistance to iodine. Recent studies showed promising results on application of iodine-containing nano-micelles against antibiotic-resistant pathogens as a supplement to antibiotic therapy. The mechanisms of action, however, remain unclear. The collection strain Escherichia coli ATCC BAA-196 showing an extended spectrum of resistance to ββ-lactam and aminoglycoside antibiotics was used in this study as a model organism. Antibiotic resistance patterns, whole genomes and total RNA sequences of the FS-1-treated (FS) and negative control (NC) variants of E. coli BAA-196 were obtained and analyzed. FS culture showed an increased susceptibility to antibiotics associated with profound gene expression alterations switching the bacterial metabolism to anaerobic respiration, increased anabolism, osmotic stress response and inhibition of many nutrient uptake systems. Nucleotide methylation pattern were identified in FS and NC cultures. While the numbers of methylated sites in both genomes remained similar, some peculiar alterations were observed in their distribution along chromosomal and plasmid sequences.

Keywords:

Papers of special note have been highlighted as: • of interest; •• of considerable interest

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Vol. 16, No. 14

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Received 19 July 2020

Accepted 10 August 2021

Published online 1 September 2021

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Supplementary data

To view the supplementary data that accompany this paper please visit the journal website at: www.futuremedicine.com/doi/suppl/10.2217/fmb-2020-0184

Author contributions

IS Korotetskiy – sequencing, data processing and visualization, manuscript writing and edition; AB Jumagaziyeva – microbiological procedures, data processing and visualization, manuscript writing and edition; SV Shilov – sequencing, data processing and visualization; TV Kuznetsova – microbiological procedures, data processing; AN Myrzabayeva – microbiological procedures, HPLC, data processing and visualization; ZA Iskakbayeva – microbiological procedures, HPLC, data processing and visualization; AI Ilin – project management and conceptualization, funding acquisition, manuscript writing and edition; M Joubert – data processing and visualization, manuscript writing and edition; S Taukobong – genome annotation; ON Reva – data processing and visualization, funding acquisition, manuscript writing and edition.

Acknowledgments

The authors would like to thank G Plunkett III, the Senior Scientist Emeritus at the University of Wisconsin–Madison, for his valuable consultations regarding the history of the strain E. coli ATCC BAA-196 used in this study as a model organism. The authors would also like to thank the laboratories of Radiobiology and Radiochemistry (SCAID) for technical support in conducting radiobiological studies of DNA and the Control Analytical Laboratory (SCAID) for technical support in conducting HPLC studies.

Financial & competing interests disclosure

All experimental procedures were funded by the grant O.0776 and BR09458960 of the program ‘Study of reversion of antibiotic resistance of pathogenic microorganisms’ provided by the Industrial Development Committee of the Ministry of Industry and Infrastructure Development of the Republic of Kazakhstan. Genome assembly, annotation, bioinformatics analysis and student support of M Joubert were funded by the South African National Research Foundation (NRF) grant 105996. The authors have no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed.

No writing assistance was utilized in the production of this manuscript.

Data sharing statement

PacBio reads generated in three repeats from the negative control (NC) and FS-1-treated E. coli ATCC BAA-196 were deposited at NCBI SRA database under accession numbers (SRX6842003, SRX6842011, SRX6842012) and (SRX6842007–SRX6842009), respectively. Two complete genome sequences of the NC and FS variants of E. coli ATCC BAA-196, which included chromosomal and plasmid sequences, were deposited at NCBI with the accession numbers CP042865-CP042866 for the NC variant of the chromosome and large plasmid of this strain; and CP042867-CP042870 for the chromosome and three plasmids of the FS variant. Three repetitions of RNA reads generated from the NC and FS variants were deposited at NCBI SRA database under accession numbers SRX6842006 and SRX6842002, respectively.

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