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References

  1. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. 2010. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8: 251-259.
    Pubmed CrossRef
  2. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J. 2009. Functional metagenomics reveals diverse betalactamases in a remote Alaskan soil. ISME J. 3: 243-251.
    Pubmed CrossRef
  3. Amann RI, Ludwig W, Schleifer KH. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59: 143-169.
    Pubmed PMC
  4. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, GriffithsJones S, et al. 2004. The Pfam protein families database. Nucleic Acids Res. 32: D138-D141.
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  5. Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P. 2007. CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8: 209.
    Pubmed PMC CrossRef
  6. Chistoserdovai L. 2010. Functional metagenomics: recent advances and future challenges. Biotechnol. Genet. Eng. Rev. 26: 335-352.
    Pubmed CrossRef
  7. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
    Pubmed CrossRef
  8. D’Costa VM, Griffiths E, Wright GD. 2007. Expanding the soil antibiotic resistome: exploring environmental diversity. Curr. Opin. Microbiol. 10: 481-489.
    Pubmed CrossRef
  9. Davies J, Wright GD. 1997. Bacterial resistance to aminoglycoside antibiotics. Trends Microbiol. 5: 234-240.
    CrossRef
  10. Demanche S, Sanguin H, Poté J, Navarro E, Bernillon D, Mavingui P, et al. 2008. Antibiotic-resistant soil bacteria in transgenic plant fields. Proc. Natl. Acad. Sci. USA 105: 3957-3962.
    Pubmed PMC CrossRef
  11. Donato JJ, Moe LA, Converse BJ, Smart KD, Berklein FC, McManus PS, Handelsman J. 2010. Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins. Appl. Environ. Microbiol. 76:4396-4401.
    Pubmed PMC CrossRef
  12. Finney DJ. 1947. Probit Analysis; A Statistical Treatment of the Sigmoid Response Curve. Cambridge University Press.
  13. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337: 1107-1111.
    Pubmed PMC CrossRef
  14. Gad GF, Mohamed HA, Ashour HM. 2011. Aminoglycoside resistance rates, phenotypes, and mechanisms of gramnegative bacteria from infected patients in upper Egypt. PLoS One 6: e17224.
    Pubmed PMC CrossRef
  15. Gerdes K, Christensen SK, Lobner-Olesen A. 2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371-382.
    Pubmed CrossRef
  16. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. 2005. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 33: D121-D124.
    Pubmed PMC CrossRef
  17. Henriques I, Moura A, Alves A, Saavedra MJ, Correia A. 2006. Analysing diversity among beta-lactamase encoding genes in aquatic environments. FEMS Microbiol. Ecol. 56: 418-429.
    Pubmed CrossRef
  18. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
    Pubmed PMC CrossRef
  19. Kim KS, Rowlinson MC, Bennion R, Liu C, Talan D, Summanen P, Finegold SM. 2010. Characterization of Slackia exigua isolated from human wound infections, including abscesses of intestinal origin. J. Clin. Microbiol. 48: 1070-1075.
    Pubmed PMC CrossRef
  20. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305: 567-580.
    Pubmed CrossRef
  21. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19: 1639-1645.
    Pubmed PMC CrossRef
  22. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35: 3100-3108.
    Pubmed PMC CrossRef
  23. Lang KS, Anderson JM, Schwarz S, Williamson L, Handelsman J, Singer RS. 2010. Novel florfenicol and chloramphenicol resistance gene discovered in Alaskan soil by using functional metagenomics. Appl. Environ. Microbiol. 76: 5321-5326.
    Pubmed PMC CrossRef
  24. Lee MH, Lee CH, Oh TK, Song JK, Yoon JH. 2006. Isolation and characterization of a novel lipase from a metagenomic library of tidal flat sediments: evidence for a new family of bacterial lipases. Appl. Environ. Microbiol. 72: 7406-7409.
    Pubmed PMC CrossRef
  25. Lee MH, Oh KH, Kang CH, Kim JH, Oh TK, Ryu CM, Yoon JH. 2012. Novel metagenome-derived, cold-adapted alkaline phospholipase with superior lipase activity as an intermediate between phospholipase and lipase. Appl. Environ. Microbiol. 78: 4959-4966.
    Pubmed PMC CrossRef
  26. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
    Pubmed PMC CrossRef
  27. Martin J, Barras M, Yui N, Kirkpatrick C, Kubler P, Norris R. 2012. Gentamicin monitoring practices in teaching hospitals - time to undertake the necessary randomised controlled trial. J. Clin. Toxicol. 2: 146.1-146.5.
  28. McHardy AC, Martin HG, Tsirigos A, Hugenholtz P, Rigoutsos I. 2007. Accurate phylogenetic classification of variable-length DNA fragments. Nat. Methods 4: 63-72.
    Pubmed CrossRef
  29. Moyed HS, Bertrand KP. 1983. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155: 768-775.
    Pubmed PMC
  30. Mullany P. 2014. Functional metagenomics for the investigation of antibiotic resistance. Virulence 5: 443-447.
    Pubmed PMC CrossRef
  31. Nagai F, Watanabe Y, Morotomi M. 2010. Slackia piriformis sp. nov. and Collinsella tanakaei sp. nov., new members of the family Coriobacteriaceae, isolated from human faeces. Int. J. Syst. Evol. Microbiol. 60: 2639-2646.
    Pubmed CrossRef
  32. Otsuka Y, Ueno H, Yonesaki T. 2003. Escherichia coli endoribonucleases involved in cleavage of bacteriophage T4 mRNAs. J. Bacteriol. 185: 983-990.
    Pubmed PMC CrossRef
  33. Otsuka Y, Yonesaki T. 2012. Dmd of bacteriophage T4 functions as an antitoxin against Escherichia coli LsoA and RnlA toxins. Mol. Microbiol. 83: 669-681.
    Pubmed CrossRef
  34. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8: 785-786.
    Pubmed CrossRef
  35. Popowska M, Rzeczycka M, Miernik A, Krawczyk-Balska A, Walsh F, Duffy B. 2012. Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob. Agents Chemother. 56: 1434-1443.
    Pubmed PMC CrossRef
  36. Pukall R, Lapidus A, Nolan M, Copeland A, Glavina Del Rio T, Lucas S, et al. 2009. Complete genome sequence of Slackia heliotrinireducens type strain (RHS 1). Stand. Genomic Sci. 1: 234-241.
    Pubmed PMC CrossRef
  37. Rath S, Sahu MC, Dubey D, Debata NK, Padhy RN. 2011. Which value should be used as the lethal concentration 50 (LC(50)) with bacteria? Interdiscipl. Sci. 3: 138-143.
    Pubmed CrossRef
  38. Riesenfeld CS, Goodman RM, Handelsman J. 2004. Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ. Microbiol. 6: 981-989.
    Pubmed CrossRef
  39. Sambrook J, Russell DW. 2006. Fragmentation of DNA by sonication. CSH Protoc. 2006. DOI: 10.1101/pdb.prot4538.
    CrossRef
  40. Schmieder R, Edwards R. 2011. Insights into antibiotic resistance through metagenomic approaches. Future Microbiol. 7: 73-89.
    Pubmed CrossRef
  41. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG. 2009. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323: 396-401.
    Pubmed PMC CrossRef
  42. Shakil S, Khan R, Zarrilli R, Khan AU. 2008. Aminoglycosides versus bacteria - a description of the action, resistance mechanism, and nosocomial battleground. J. Biomed. Sci. 15:5-14.
    Pubmed CrossRef
  43. Shaw KJ, Rather PN, Hare RS, Miller GH. 1993. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol. Rev. 57: 138-163.
    Pubmed PMC
  44. Tao W, Lee MH, Wu J, Kim NH, Kim JC, Chung E, et al. 2012. Inactivation of chloramphenicol and florfenicol by a novel chloramphenicol hydrolase. Appl. Environ. Microbiol. 78: 6295-6301.
    Pubmed PMC CrossRef
  45. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, et al. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
    Pubmed PMC CrossRef
  46. Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, et al. 2005. Comparative metagenomics of microbial communities. Science 308: 554-557.
    Pubmed CrossRef
  47. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74.
    Pubmed CrossRef
  48. Wade WG, Downes J, Dymock D, Hiom SJ, Weightman AJ, Dewhirst FE, et al. 1999. The family Coriobacteriaceae:reclassification of Eubacterium exiguum (Poco et al. 1996) and Peptostreptococcus heliotrinireducens (Lanigan 1976) as Slackia exigua gen. nov., comb. nov. and Slackia heliotrinireducens gen. nov., comb. nov., and Eubacterium lentum (Prevot 1938) as Eggerthella lenta gen. nov., comb. nov. Int. J. Syst. Bacteriol. 49: 595-600.
    Pubmed CrossRef
  49. Wiegand I, Hilpert K, Hancock RE. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3: 163-175.
    Pubmed CrossRef
  50. Williams JJ, Hergenrother PJ. 2012. Artificial activation of toxin-antitoxin systems as an antibacterial strategy. Trends Microbiol. 20: 291-298.
    Pubmed PMC CrossRef
  51. Wu CH, Apweiler R, Bairoch A, Natale DA, Barker WC, Boeckmann B, et al. 2006. The Universal Protein Resource (UniProt): an expanding universe of protein information. Nucleic Acids Res. 34: D187-D191.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2016; 26(3): 521-529

Published online March 28, 2016 https://doi.org/10.4014/jmb.1511.11053

Copyright © The Korean Society for Microbiology and Biotechnology.

Functional Metagenome Mining of Soil for a Novel Gentamicin Resistance Gene

Hyunjoo Im 1, 2, Kyung Mo Kim 3, 4, Sang-Heon Lee 3, 4 and Choong-Min Ryu 1, 2*

1Molecular Phytobacteriology Laboratory, KRIBB, Daejeon 34113, Republic of Korea, 2Biosystems and Bioengineering Program, University of Science and Technology (UST), Daejeon 34141, Republic of Korea, 3Microbial Resource Center, KRIBB, Jeongeup 56212, Republic of Korea, 4Department of Bioinformatics, University of Science and Technology (UST), Daejeon 34141, Republic of Korea

Received: November 19, 2015; Accepted: December 10, 2015

Abstract

Extensive use of antibiotics over recent decades has led to bacterial resistance against
antibiotics, including gentamicin, one of the most effective aminoglycosides. The emergence of
resistance is problematic for hospitals, since gentamicin is an important broad-spectrum
antibiotic for the control of bacterial pathogens in the clinic. Previous study to identify
gentamicin resistance genes from environmental samples have been conducted using culturedependent screening methods. To overcome these limitations, we employed a metagenomebased culture-independent protocol to identify gentamicin resistance genes. Through
functional screening of metagenome libraries derived from soil samples, a fosmid clone was
selected as it conferred strong gentamicin resistance. To identify a specific functioning gene
conferring gentamicin resistance from a selected fosmid clone (35–40 kb), a shot-gun library
was constructed and four shot-gun clones (2–3 kb) were selected. Further characterization of
these clones revealed that they contained sequences similar to that of the RNA ligase, T4 rnlA
that is known as a toxin gene. The overexpression of the rnlA-like gene in Escherichia coli
increased gentamicin resistance, indicating that this toxin gene modulates this trait. The results
of our metagenome library analysis suggest that the rnlA-like gene may represent a new class of
gentamicin resistance genes in pathogenic bacteria. In addition, we demonstrate that the soil
metagenome can provide an important resource for the identification of antibiotic resistance
genes, which are valuable molecular targets in efforts to overcome antibiotic resistance.

Keywords: Gentamicin, Metagenome, Antibiotic-resistance, RnlA, Shot-gun library

References

  1. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. 2010. Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8: 251-259.
    Pubmed CrossRef
  2. Allen HK, Moe LA, Rodbumrer J, Gaarder A, Handelsman J. 2009. Functional metagenomics reveals diverse betalactamases in a remote Alaskan soil. ISME J. 3: 243-251.
    Pubmed CrossRef
  3. Amann RI, Ludwig W, Schleifer KH. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59: 143-169.
    Pubmed KoreaMed
  4. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, GriffithsJones S, et al. 2004. The Pfam protein families database. Nucleic Acids Res. 32: D138-D141.
    Pubmed KoreaMed CrossRef
  5. Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P. 2007. CRISPR recognition tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8: 209.
    Pubmed KoreaMed CrossRef
  6. Chistoserdovai L. 2010. Functional metagenomics: recent advances and future challenges. Biotechnol. Genet. Eng. Rev. 26: 335-352.
    Pubmed CrossRef
  7. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
    Pubmed CrossRef
  8. D’Costa VM, Griffiths E, Wright GD. 2007. Expanding the soil antibiotic resistome: exploring environmental diversity. Curr. Opin. Microbiol. 10: 481-489.
    Pubmed CrossRef
  9. Davies J, Wright GD. 1997. Bacterial resistance to aminoglycoside antibiotics. Trends Microbiol. 5: 234-240.
    CrossRef
  10. Demanche S, Sanguin H, Poté J, Navarro E, Bernillon D, Mavingui P, et al. 2008. Antibiotic-resistant soil bacteria in transgenic plant fields. Proc. Natl. Acad. Sci. USA 105: 3957-3962.
    Pubmed KoreaMed CrossRef
  11. Donato JJ, Moe LA, Converse BJ, Smart KD, Berklein FC, McManus PS, Handelsman J. 2010. Metagenomic analysis of apple orchard soil reveals antibiotic resistance genes encoding predicted bifunctional proteins. Appl. Environ. Microbiol. 76:4396-4401.
    Pubmed KoreaMed CrossRef
  12. Finney DJ. 1947. Probit Analysis; A Statistical Treatment of the Sigmoid Response Curve. Cambridge University Press.
  13. Forsberg KJ, Reyes A, Wang B, Selleck EM, Sommer MO, Dantas G. 2012. The shared antibiotic resistome of soil bacteria and human pathogens. Science 337: 1107-1111.
    Pubmed KoreaMed CrossRef
  14. Gad GF, Mohamed HA, Ashour HM. 2011. Aminoglycoside resistance rates, phenotypes, and mechanisms of gramnegative bacteria from infected patients in upper Egypt. PLoS One 6: e17224.
    Pubmed KoreaMed CrossRef
  15. Gerdes K, Christensen SK, Lobner-Olesen A. 2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371-382.
    Pubmed CrossRef
  16. Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A. 2005. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 33: D121-D124.
    Pubmed KoreaMed CrossRef
  17. Henriques I, Moura A, Alves A, Saavedra MJ, Correia A. 2006. Analysing diversity among beta-lactamase encoding genes in aquatic environments. FEMS Microbiol. Ecol. 56: 418-429.
    Pubmed CrossRef
  18. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ. 2010. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119.
    Pubmed KoreaMed CrossRef
  19. Kim KS, Rowlinson MC, Bennion R, Liu C, Talan D, Summanen P, Finegold SM. 2010. Characterization of Slackia exigua isolated from human wound infections, including abscesses of intestinal origin. J. Clin. Microbiol. 48: 1070-1075.
    Pubmed KoreaMed CrossRef
  20. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305: 567-580.
    Pubmed CrossRef
  21. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, et al. 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19: 1639-1645.
    Pubmed KoreaMed CrossRef
  22. Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35: 3100-3108.
    Pubmed KoreaMed CrossRef
  23. Lang KS, Anderson JM, Schwarz S, Williamson L, Handelsman J, Singer RS. 2010. Novel florfenicol and chloramphenicol resistance gene discovered in Alaskan soil by using functional metagenomics. Appl. Environ. Microbiol. 76: 5321-5326.
    Pubmed KoreaMed CrossRef
  24. Lee MH, Lee CH, Oh TK, Song JK, Yoon JH. 2006. Isolation and characterization of a novel lipase from a metagenomic library of tidal flat sediments: evidence for a new family of bacterial lipases. Appl. Environ. Microbiol. 72: 7406-7409.
    Pubmed KoreaMed CrossRef
  25. Lee MH, Oh KH, Kang CH, Kim JH, Oh TK, Ryu CM, Yoon JH. 2012. Novel metagenome-derived, cold-adapted alkaline phospholipase with superior lipase activity as an intermediate between phospholipase and lipase. Appl. Environ. Microbiol. 78: 4959-4966.
    Pubmed KoreaMed CrossRef
  26. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25: 955-964.
    Pubmed KoreaMed CrossRef
  27. Martin J, Barras M, Yui N, Kirkpatrick C, Kubler P, Norris R. 2012. Gentamicin monitoring practices in teaching hospitals - time to undertake the necessary randomised controlled trial. J. Clin. Toxicol. 2: 146.1-146.5.
  28. McHardy AC, Martin HG, Tsirigos A, Hugenholtz P, Rigoutsos I. 2007. Accurate phylogenetic classification of variable-length DNA fragments. Nat. Methods 4: 63-72.
    Pubmed CrossRef
  29. Moyed HS, Bertrand KP. 1983. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155: 768-775.
    Pubmed KoreaMed
  30. Mullany P. 2014. Functional metagenomics for the investigation of antibiotic resistance. Virulence 5: 443-447.
    Pubmed KoreaMed CrossRef
  31. Nagai F, Watanabe Y, Morotomi M. 2010. Slackia piriformis sp. nov. and Collinsella tanakaei sp. nov., new members of the family Coriobacteriaceae, isolated from human faeces. Int. J. Syst. Evol. Microbiol. 60: 2639-2646.
    Pubmed CrossRef
  32. Otsuka Y, Ueno H, Yonesaki T. 2003. Escherichia coli endoribonucleases involved in cleavage of bacteriophage T4 mRNAs. J. Bacteriol. 185: 983-990.
    Pubmed KoreaMed CrossRef
  33. Otsuka Y, Yonesaki T. 2012. Dmd of bacteriophage T4 functions as an antitoxin against Escherichia coli LsoA and RnlA toxins. Mol. Microbiol. 83: 669-681.
    Pubmed CrossRef
  34. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8: 785-786.
    Pubmed CrossRef
  35. Popowska M, Rzeczycka M, Miernik A, Krawczyk-Balska A, Walsh F, Duffy B. 2012. Influence of soil use on prevalence of tetracycline, streptomycin, and erythromycin resistance and associated resistance genes. Antimicrob. Agents Chemother. 56: 1434-1443.
    Pubmed KoreaMed CrossRef
  36. Pukall R, Lapidus A, Nolan M, Copeland A, Glavina Del Rio T, Lucas S, et al. 2009. Complete genome sequence of Slackia heliotrinireducens type strain (RHS 1). Stand. Genomic Sci. 1: 234-241.
    Pubmed KoreaMed CrossRef
  37. Rath S, Sahu MC, Dubey D, Debata NK, Padhy RN. 2011. Which value should be used as the lethal concentration 50 (LC(50)) with bacteria? Interdiscipl. Sci. 3: 138-143.
    Pubmed CrossRef
  38. Riesenfeld CS, Goodman RM, Handelsman J. 2004. Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ. Microbiol. 6: 981-989.
    Pubmed CrossRef
  39. Sambrook J, Russell DW. 2006. Fragmentation of DNA by sonication. CSH Protoc. 2006. DOI: 10.1101/pdb.prot4538.
    CrossRef
  40. Schmieder R, Edwards R. 2011. Insights into antibiotic resistance through metagenomic approaches. Future Microbiol. 7: 73-89.
    Pubmed CrossRef
  41. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG. 2009. Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science 323: 396-401.
    Pubmed KoreaMed CrossRef
  42. Shakil S, Khan R, Zarrilli R, Khan AU. 2008. Aminoglycosides versus bacteria - a description of the action, resistance mechanism, and nosocomial battleground. J. Biomed. Sci. 15:5-14.
    Pubmed CrossRef
  43. Shaw KJ, Rather PN, Hare RS, Miller GH. 1993. Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol. Rev. 57: 138-163.
    Pubmed KoreaMed
  44. Tao W, Lee MH, Wu J, Kim NH, Kim JC, Chung E, et al. 2012. Inactivation of chloramphenicol and florfenicol by a novel chloramphenicol hydrolase. Appl. Environ. Microbiol. 78: 6295-6301.
    Pubmed KoreaMed CrossRef
  45. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, et al. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41.
    Pubmed KoreaMed CrossRef
  46. Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, et al. 2005. Comparative metagenomics of microbial communities. Science 308: 554-557.
    Pubmed CrossRef
  47. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, et al. 2004. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74.
    Pubmed CrossRef
  48. Wade WG, Downes J, Dymock D, Hiom SJ, Weightman AJ, Dewhirst FE, et al. 1999. The family Coriobacteriaceae:reclassification of Eubacterium exiguum (Poco et al. 1996) and Peptostreptococcus heliotrinireducens (Lanigan 1976) as Slackia exigua gen. nov., comb. nov. and Slackia heliotrinireducens gen. nov., comb. nov., and Eubacterium lentum (Prevot 1938) as Eggerthella lenta gen. nov., comb. nov. Int. J. Syst. Bacteriol. 49: 595-600.
    Pubmed CrossRef
  49. Wiegand I, Hilpert K, Hancock RE. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3: 163-175.
    Pubmed CrossRef
  50. Williams JJ, Hergenrother PJ. 2012. Artificial activation of toxin-antitoxin systems as an antibacterial strategy. Trends Microbiol. 20: 291-298.
    Pubmed KoreaMed CrossRef
  51. Wu CH, Apweiler R, Bairoch A, Natale DA, Barker WC, Boeckmann B, et al. 2006. The Universal Protein Resource (UniProt): an expanding universe of protein information. Nucleic Acids Res. 34: D187-D191.
    Pubmed KoreaMed CrossRef