Skip to main content

Advertisement

Log in

Marine Sediment Bacteria Harbor Antibiotic Resistance Genes Highly Similar to Those Found in Human Pathogens

  • Microbiology of Aquatic Systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The ocean is a natural habitat for antibiotic-producing bacteria, and marine aquaculture introduces antibiotics into the ocean to treat infections and improve aquaculture production. Studies have shown that the ocean is an important reservoir of antibiotic resistance genes. However, there is a lack of understanding and knowledge about the clinical importance of the ocean resistome. We investigated the relationship between the ocean bacterial resistome and pathogenic resistome. We applied high-throughput sequencing and metagenomic analyses to explore the resistance genes in bacterial plasmids from marine sediments. Numerous putative resistance determinants were detected among the resistance genes in the sediment bacteria. We also found that several contigs shared high identity with transposons or plasmids from human pathogens, indicating that the sediment bacteria recently contributed or acquired resistance genes from pathogens. Marine sediment bacteria could play an important role in the global exchange of antibiotic resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. D'Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Sci 311(5759):374–377. doi:10.1126/science.1120800

    Article  Google Scholar 

  2. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Sci 337(6098):1107–1111. doi:10.1126/science.1220761

    Article  CAS  Google Scholar 

  3. Brown Kav A, Sasson G, Jami E, Doron-Faigenboim A, Benhar I, Mizrahi I (2012) Insights into the bovine rumen plasmidome. Proc Natl Acad Sci USA 14(109):7

    Google Scholar 

  4. Szczepanowski R, Bekel T, Goesmann A, Krause L, Krömeke H, Kaiser O, Eichler W, Pühler A, Schlüter A (2008) Insight into the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to antimicrobial drugs analysed by the 454-pyrosequencing technology. J Biotechnol 136:11

    Article  Google Scholar 

  5. Zhang T, Zhang XX, Ye L (2011) Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLoS One 6(10):e26041. doi:10.1371/journal.pone.0026041

    Article  PubMed  CAS  Google Scholar 

  6. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    PubMed  CAS  Google Scholar 

  7. Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A (2010) Manipulation of FASTQ data with Galaxy. Bioinforma 26(14):1783–1785. doi:10.1093/bioinformatics/btq281

    Article  CAS  Google Scholar 

  8. Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18(5):821–829. doi:10.1101/gr.074492.107

    Article  PubMed  CAS  Google Scholar 

  9. Ma Y, Paulsen IT, Palenik B (2012) Analysis of two marine metagenomes reveals the diversity of plasmids in oceanic environments. Environ Microbiol 14(2):453–466. doi:10.1111/j.1462-2920.2011.02633.x

    Article  PubMed  Google Scholar 

  10. Sonnhammer EL, Eddy SR, Birney E, Bateman A, Durbin R (1998) Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res 26(1):320–322

    Article  PubMed  CAS  Google Scholar 

  11. Liu B, Pop M (2009) ARDB—Antibiotic Resistance Genes Database. Nucleic Acids Res 37:D443–447. doi:10.1093/nar/gkn656

    Article  PubMed  CAS  Google Scholar 

  12. Seyfried EE, Newton RJ, Rubert KF, Pedersen JA, McMahon KD (2010) Occurrence of tetracycline resistance genes in aquaculture facilities with varying use of oxytetracycline. Microb Ecol 59(4):799–807. doi:10.1007/s00248-009-9624-7

    Article  PubMed  CAS  Google Scholar 

  13. Gao P, Mao D, Luo Y, Wang L, Xu B, Xu L (2012) Occurrence of sulfonamide and tetracycline-resistant bacteria and resistance genes in aquaculture environment. Water Res 46(7):2355–2364. doi:10.1016/j.watres.2012.02.004

    Article  PubMed  CAS  Google Scholar 

  14. Di Cesare A, Vignaroli C, Luna GM, Pasquaroli S, Biavasco F (2012) Antibiotic-resistant enterococci in seawater and sediments from a coastal fish farm. Microb Drug Resist. doi:10.1089/mdr.2011.0204

  15. Tamminen M, Karkman A, Lohmus A, Muziasari WI, Takasu H, Wada S, Suzuki S, Virta M (2011) Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. Environ Sci Technol 45(2):386–391. doi:10.1021/es102725n

    Article  PubMed  CAS  Google Scholar 

  16. Dang H, Ren J, Song L, Sun S, An L (2008) Diverse tetracycline resistant bacteria and resistance genes from coastal waters of Jiaozhou Bay. Microb Ecol 55(2):237–246. doi:10.1007/s00248-007-9271-9

    Article  PubMed  CAS  Google Scholar 

  17. Akiyama T, Khan AA (2012) Molecular characterization of strains of fluoroquinolone-resistant Salmonella enterica serovar Schwarzengrund carrying multidrug resistance isolated from imported foods. J Antimicrob Chemother 67(1):101–110. doi:10.1093/jac/dkr414

    Article  PubMed  CAS  Google Scholar 

  18. Nordmann P, Poirel L (2005) Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J Antimicrob Chemother 56(3):463–469. doi:10.1093/jac/dki245

    Article  PubMed  CAS  Google Scholar 

  19. Poirel L, Rodriguez-Martinez JM, Mammeri H, Liard A, Nordmann P (2005) Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob Agents Chemother 49(8):3523–3525. doi:10.1128/AAC.49.8.3523-3525.2005

    Article  PubMed  CAS  Google Scholar 

  20. L'Abee-Lund TM, Sorum H (2000) Functional Tn5393-like transposon in the R plasmid pRAS2 from the fish pathogen Aeromonas salmonicida subspecies salmonicida isolated in Norway. Appl Environ Microbiol 66(12):5533–5535

    Article  PubMed  Google Scholar 

  21. Ambrose KD, Nisbet R, Stephens DS (2005) Macrolide efflux in Streptococcus pneumoniae is mediated by a dual efflux pump (mel and mef) and is erythromycin inducible. Antimicrob Agents Chemother 49(10):4203–4209. doi:10.1128/AAC.49.10.4203-4209.2005

    Article  PubMed  CAS  Google Scholar 

  22. Kehrenberg C, Schwarz S (2006) Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates. Antimicrob Agents Chemother 50(4):1156–1163. doi:10.1128/AAC.50.4.1156-1163.2006

    Article  PubMed  CAS  Google Scholar 

  23. Murray KD, Aronstein KA, de Leon JH (2007) Analysis of pMA67, a predicted rolling-circle replicating, mobilizable, tetracycline-resistance plasmid from the honey bee pathogen, Paenibacillus larvae. Plasmid 58(2):89–100. doi:10.1016/j.plasmid.2007.02.001

    Article  PubMed  CAS  Google Scholar 

  24. You Y, Hilpert M, Ward MJ (2012) Detection of a common and persistent tet(L)-carrying plasmid in chicken-waste-impacted farm soil. Appl Environ Microbiol 78(9):3203–3213. doi:10.1128/AEM.07763-11

    Article  PubMed  CAS  Google Scholar 

  25. Akinbowale OL, Peng H, Barton MD (2007) Diversity of tetracycline resistance genes in bacteria from aquaculture sources in Australia. J Appl Microbiol 103(5):2016–2025. doi:10.1111/j.1365-2672.2007.03445.x

    Article  PubMed  CAS  Google Scholar 

  26. Zhao JY, Dang H (2012) Coastal seawater bacteria harbor a large reservoir of plasmid-mediated quinolone resistance determinants in Jiaozhou Bay, China. Microb Ecol 64(1):187–199. doi:10.1007/s00248-012-0008-z

    Article  PubMed  CAS  Google Scholar 

  27. Verner-Jeffreys DW, Welch TJ, Schwarz T, Pond MJ, Woodward MJ, Haig SJ, Rimmer GS, Roberts E, Morrison V, Baker-Austin C (2009) High prevalence of multidrug-tolerant bacteria and associated antimicrobial resistance genes isolated from ornamental fish and their carriage water. PLoS One 4(12):e8388. doi:10.1371/journal.pone.0008388

    Article  PubMed  Google Scholar 

  28. Mantengoli E, Rossolini GM (2005) Tn5393d, a complex Tn5393 derivative carrying the PER-1 extended-spectrum beta-lactamase gene and other resistance determinants. Antimicrob Agents Chemother 49(8):3289–3296. doi:10.1128/AAC.49.8.3289-3296.2005

    Article  PubMed  CAS  Google Scholar 

  29. Petrovski S, Stanisich VA (2011) Embedded elements in the IncPbeta plasmids R772 and R906 can be mobilized and can serve as a source of diverse and novel elements. Microbiol 157(Pt 6):1714–1725. doi:10.1099/mic.0.047761-0

    CAS  Google Scholar 

  30. Miriagou V, Papagiannitsis CC, Kotsakis SD, Loli A, Tzelepi E, Legakis NJ, Tzouvelekis LS (2010) Sequence of pNL194, a 79.3-kilobase IncN plasmid carrying the blaVIM-1 metallo-beta-lactamase gene in Klebsiella pneumoniae. Antimicrob Agents Chemother 54(10):4497–4502. doi:10.1128/AAC.00665-10

    Article  PubMed  CAS  Google Scholar 

  31. Del Grosso M, Camilli R, Iannelli F, Pozzi G, Pantosti A (2006) The mef(E)-carrying genetic element (mega) of Streptococcus pneumoniae: insertion sites and association with other genetic elements. Antimicrob Agents Chemother 50(10):3361–3366. doi:10.1128/AAC.00277-06

    Article  PubMed  Google Scholar 

  32. Zhanel GG, Wang X, Nichol K, Nikulin A, Wierzbowski AK, Mulvey M, Hoban DJ (2006) Molecular characterisation of Canadian paediatric multidrug-resistant Streptococcus pneumoniae from 1998–2004. Int J Antimicrob Agents 28(5):465–471. doi:10.1016/j.ijantimicag.2006.08.005

    Article  PubMed  CAS  Google Scholar 

  33. Jonsson M, Swedberg G (2006) Macrolide resistance can be transferred by conjugation from viridans streptococci to Streptococcus pyogenes. Int J Antimicrob Agents 28(2):101–103. doi:10.1016/j.ijantimicag.2006.02.023

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Knowledge Innovation Program of the Chinese Academy of Sciences (grant no. KSCX2-EW-J-6) and the National High-Technology Research and Development Program (“863” Program) of China (grant no. 2012AA092001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jie Feng.

Additional information

Jing Yang, Chao Wang, and Chang Shu contributed to this work equally.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yang, J., Wang, C., Shu, C. et al. Marine Sediment Bacteria Harbor Antibiotic Resistance Genes Highly Similar to Those Found in Human Pathogens. Microb Ecol 65, 975–981 (2013). https://doi.org/10.1007/s00248-013-0187-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0187-2

Keywords

Navigation