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Volume 167, Issue 12

gene diversity in spp. Free

Abstract

Members of are ubiquitous in aquatic environments, some of which have been implicated in human infections. The progenitors of antibiotic resistance genes with clinical relevance, such as genes, have been identified in code for a pentapeptide repeat protein that protects type II topoisomerases, decreasing susceptibility to quinolones and fluoroquinolones. In this study, 248 genomes of 49 species were analysed as well as 33 environmental isolates belonging to 10 species. The presence of the gene was detected in 22.9% of the genomes and 15.2% of the isolates. The gene was more often detected in , but was also detected in , , and . The identified genes encoded the previously described variants QnrA3 (in 22 genomes of one species), QnrA2 (eight genomes and three species), QnrA1 (six genomes and two species), QnrA7 (five genomes and two species), QnrA10 (two genomes of one species) and QnrA4 (one genome). In addition, 11 novel variants with 3 to 7 amino acid substitutions were identified (in 13 genomes and one environmental isolate). The presence of this gene appears to be species-specific although within some species several variants were detected. The study presents a previously unknown diversity of in , highlighting the role of this genus as progenitor and reservoir of these genes. Further studies are needed to determine the phenotypes conferred by the new variants and the mechanisms that may mediate the transfer of these genes to new hosts.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): environmental Shewanella , gene progenitor , qnrA gene and quinolone resistance
Funding
This study was supported by the:
  • Fundação para a Ciência e a Tecnologia (Award SFRH/BD/52573/2014)
    • Principle Award Recipient: AraújoSusana
  • Fundação para a Ciência e a Tecnologia (Award CEECIND/00977/2020)
    • Principle Award Recipient: TacãoMarta
  • Fundação para a Ciência e a Tecnologia (Award UIDP/50017/2020+UIDB/50017/2020)
    • Principle Award Recipient: ApplicableNot
© 2021 The Authors
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2021-12-16
2024-04-25
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References

  1. Pham TDM, Ziora ZM, Blaskovich MAT. Quinolone antibiotics. Medchemcomm 2019; 10:1719–1739 [View Article] [PubMed]
     [Google Scholar]
  2. Janecko N, Pokludova L, Blahova J, Svobodova Z, Literak I. Implications of fluoroquinolone contamination for the aquatic environment-A review. Environ Toxicol Chem 2016; 35:2647–2656 [View Article] [PubMed]
     [Google Scholar]
  3. Nordmann P, Poirel L. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 2005; 56:463–469 [View Article]
     [Google Scholar]
  4. Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A. Plasmid-mediated quinolone resistance: An update. J Infect Chemother 2011; 17:149–182 [View Article] [PubMed]
     [Google Scholar]
  5. Girijan SK, Paul R, V J RK, Pillai D. Investigating the impact of hospital antibiotic usage on aquatic environment and aquaculture systems: A molecular study of quinolone resistance in Escherichia coli. Sci Total Environ 2020; 748:141538 [View Article] [PubMed]
     [Google Scholar]
  6. Poirel L, Cattoir V, Nordmann P. Is plasmid-mediated quinolone resistance a clinically significant problem?. Clin Microbiol Infect 2008; 14:295–297 [View Article]
     [Google Scholar]
  7. Périchon B, Courvalin P, Galimand M. Transferable resistance to aminoglycosides by methylation of G1405 in 16S rRNA and to hydrophilic fluoroquinolones by QepA-mediated efflux in Escherichia coli. Antimicrob Agents Chemother 2007; 51:2464–2469 [View Article] [PubMed]
     [Google Scholar]
  8. Yamane K, Wachino J, Suzuki S, Kimura K, Shibata N et al. New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother 2007; 51:3354–3360 [View Article] [PubMed]
     [Google Scholar]
  9. Cattoir V, Nordmann P. Plasmid-mediated quinolone resistance in Gram-negative bacterial species: An update. Curr Med Chem 2009; 16:1028–1046 [View Article] [PubMed]
     [Google Scholar]
  10. Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 2007; 60:394–397 [View Article] [PubMed]
     [Google Scholar]
  11. Jacoby GA, Strahilevitz J, Hooper DC. Plasmid-mediated quinolone resistance. Microbiol Spectr 2014; 2:1–42 [View Article] [PubMed]
     [Google Scholar]
  12. Melvold JA, Wyrsch ER, McKinnon J, Roy Chowdhury P, Charles IG et al. Identification of a novel qnrA allele, qnrA8, in environmental Shewanella algae. J Antimicrob Chemother 2017; 72:2949–2952 [View Article] [PubMed]
     [Google Scholar]
  13. Tran JH, Jacoby GA. Mechanism of plasmid-mediated quinolone resistance. Proceedings of the National Academy of Sciences 2002; 99:5638–5642 [View Article] [PubMed]
     [Google Scholar]
  14. Poirel L, Rodriguez-Martinez JM, Mammeri H, Liard A, Nordmann P. Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob Agents Chemother 2005; 49:3523–3525 [View Article] [PubMed]
     [Google Scholar]
  15. Wattam AR, Davis JJ, Assaf R, Boisvert S, Brettin T et al. Improvements to PATRIC, the all-bacterial bioinformatics database and analysis resource center. Nucleic Acids Res 2017; 45:D535–D542 [View Article] [PubMed]
     [Google Scholar]
  16. Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet 1998; 351:797–799 [View Article] [PubMed]
     [Google Scholar]
  17. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182. [View Article] [PubMed]
     [Google Scholar]
  18. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S et al. NCBI BLAST: a better web interface. Nucleic Acids Res 2008; 36:W5–9 [View Article] [PubMed]
     [Google Scholar]
  19. Tacão M, Araújo S, Vendas M, Alves A, Henriques I. . Shewanella species as the origin of blaOXA-48 genes: insights into gene diversity, associated phenotypes and possible transfer mechanisms. Int J Antimicrob Agents 2018; 51:340–348 [View Article] [PubMed]
     [Google Scholar]
  20. Fidalgo C, Henriques I, Rocha J, Tacão M, Alves A. Culturable endophytic bacteria from the salt marsh plant Halimione portulacoides: phylogenetic diversity, functional characterization, and influence of metal(loid) contamination. Environ Sci Pollut Res 2016; 23:10200–10214 [View Article]
     [Google Scholar]
  21. Azevedo JSN, Ramos I, Araújo S, Oliveira CS, Correia A et al. Spatial and temporal analysis of estuarine bacterioneuston and bacterioplankton using culture-dependent and culture-independent methodologies. Antonie van Leeuwenhoek 2012; 101:819–835 [View Article]
     [Google Scholar]
  22. Leite L, Jude-Lemeilleur F, Raymond N, Henriques I, Garabetian F et al. Phylogenetic diversity and functional characterization of the Manila clam microbiota: a culture-based approach. Environ Sci Pollut Res 2017; 24:21721–21732 [View Article]
     [Google Scholar]
  23. Guillard T, Moret H, Brasme L, Carlier A, Vernet-Garnier V et al. Rapid detection of qnr and qepA plasmid-mediated quinolone resistance genes using real-time PCR. Diagn Microbiol Infect Dis 2011; 70:253–259 [View Article] [PubMed]
     [Google Scholar]
  24. Antonelli A, Di Palo DM, Galano A, Becciani S, Montagnani C et al. Intestinal carriage of Shewanella xiamenensis simulating carriage of OXA-48-producing Enterobacteriaceae. Diagn Microbiol Infect Dis 2015; 82:1–3 [View Article] [PubMed]
     [Google Scholar]
  25. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
     [Google Scholar]
  26. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539. [View Article] [PubMed]
     [Google Scholar]
  27. Lemaire ON, Méjean V, Iobbi-Nivol C. The Shewanella genus: ubiquitous organisms sustaining and preserving aquatic ecosystems. FEMS Microbiol Rev 2020; 44:155–170 [View Article] [PubMed]
     [Google Scholar]
  28. Gao H, Obraztova A, Stewart N, Popa R, Fredrickson JK et al. Shewanella loihica sp. nov., isolated from iron-rich microbial mats in the Pacific Ocean. Int J Syst Evol Microbiol 2006; 56:1911–1916 [View Article] [PubMed]
     [Google Scholar]
  29. Janda JM. Shewanella: A marine pathogen as an emerging cause of human disease. Clinical Microbiology Newsletter 2014; 36:25–29 [View Article]
     [Google Scholar]
  30. Tsai MS, You HL, Tang YF, Liu JW. . Shewanella soft tissue infection: case report and literature review. Int J Infect Dis 2008; 12:e119–e124 [View Article]
     [Google Scholar]
  31. Tseng S-Y, Liu P-Y, Lee Y-H, Wu Z-Y, Huang C-C et al. The pathogenicity of Shewanella algae and ability to tolerate a wide range of temperatures and salinities. Can J Infect Dis Med Microbiol 2018; 2018:6976897 [View Article] [PubMed]
     [Google Scholar]
  32. Zong Z. Nosocomial peripancreatic infection associated with Shewanella xiamenensis. J Med Microbiol 2011; 60:1387–1390 [View Article] [PubMed]
     [Google Scholar]
  33. Poovorawan K, Chatsuwan T, Lakananurak N, Chansaenroj J, Komolmit P et al. Shewanella haliotis associated with severe soft tissue infection, Thailand, 2012. Emerg Infect Dis 2013; 19:1019–1021 [View Article] [PubMed]
     [Google Scholar]
  34. Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA et al. Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 1999; 49 Pt 2:705–724 [View Article] [PubMed]
     [Google Scholar]
  35. Szeinbaum N, Kellum CE, Glass JB, Janda JM, DiChristina TJ. Whole-genome sequencing reveals that Shewanella haliotis Kim et al. 2007 can be considered a later heterotypic synonym of Shewanella algae Simidu et al. 1990. Int J Syst Evol Microbiol 2018; 68:1356–1360 [View Article] [PubMed]
     [Google Scholar]
  36. Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A. Plasmid-mediated quinolone resistance: A multifaceted threat. Clin Microbiol Rev 2009; 22:664–689 [View Article] [PubMed]
     [Google Scholar]
  37. Zhao J, Mu X, Zhu Y, Xi L, Xiao Z et al. Identification of an integron containing the quinolone resistance gene qnrA1 in Shewanella xiamenensis. FEMS Microbiology Letters 2015; 362:fnv146 [View Article]
     [Google Scholar]
  38. Thorell K, Meier-Kolthoff JP, Sjöling Å, Martín-Rodríguez AJ. Whole-Genome Sequencing redefines Shewanella taxonomy. Front Microbiol 2019; 10:1861. [View Article] [PubMed]
     [Google Scholar]
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qnrA gene diversity in Shewanella spp.
Microbiology 167, 001118 (2021); https://doi.org/10.1099/mic.0.001118
/content/journal/micro/10.1099/mic.0.001118
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