Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Pal, Chandan ^a   Bengtsson Palme, Johan ^a   Kristiansson, Erik ^b   Larsson, D G Joakim ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Antibiotic resistance; Bacterial genomes; Biocide resistance; Co selection; Metal resistance; Plasmids; Toxin antitoxin

Indexed keywords

AMMONIA; BIOCIDE; AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; ANTITOXIN; BACTERIAL TOXIN; DISINFECTANT AGENT; METAL; SULFONAMIDE;

ANTIBIOTIC RESISTANCE GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BIOCIDE METAL RESISTANCE GENE; CONTROLLED STUDY; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE SEQUENCE; GENETIC SELECTION; GENOME ANALYSIS; HETEROZYGOSITY; NONHUMAN; TAXONOMY; ANTIBIOTIC RESISTANCE; BACTERIUM; DRUG EFFECTS; ENVIRONMENT; GENETIC DATABASE; GENETICS; GENOMICS; HUMAN; METABOLISM; MOLECULAR EVOLUTION; PLASMID;

AMINOGLYCOSIDES; ANTI-BACTERIAL AGENTS; ANTITOXINS; BACTERIA; BACTERIAL TOXINS; BETA-LACTAM RESISTANCE; DATABASES, GENETIC; DISINFECTANTS; DRUG RESISTANCE, MICROBIAL; ENVIRONMENT; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENOMICS; HUMANS; METALS; PLASMIDS; SELECTION, GENETIC; SULFONAMIDES;

EID: 84946962704     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-2153-5     Document Type: Article

References (68)

1. Levy SB. Factors impacting on the problem of antibiotic resistance. J Antimicrob Chemother. 2002;49:25-30.
2. Wright GD. The antibiotic resistome. Expert Opin Drug Discov. 2010;5:779-88.
3. SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks). Assessment of the Antibiotic Resistance Effects of Biocides. Brussels: European Commission; 2009. p. 1-87.
4. Chapman JS. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegrad. 2003;51:271-6.
5. Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV. Co-selection of antibiotic and metal resistance. Trends Microbiol. 2006;14:176-82.
6. Piddock LJV. The crisis of no new antibiotics--what is the way forward? Lancet Infect Dis. 2012;12:249-53.
7. Olson AB, Silverman M, Boyd DA, McGeer A, Willey BM, Porter VP, et al. Identification of a progenitor of the CTX-M-9 group of extended-spectrum beta-lactamases from Kluyvera georgiana isolated in Guyana. Antimicrob Agents Chemother. 2005;49:2112-5.
8. Kümmerer K. Resistance in the environment. J Antimicrob Chemother. 2004;54:311-20.
9. Flach CF, Johnning A, Nilsson I, Smalla K, Kristiansson E, Larsson DGJ. Isolation of novel IncA/C and IncN fluoroquinolone resistance plasmids from an antibiotic-polluted lake. J Antimicrob Chemother. 2015;70:2709-17.
10. Rossolini GM, D'Andrea MM, Mugnaioli C. The spread of CTX-M-type extended-spectrum beta-lactamases. Clin Microbiol Infect. 2008;14:33-41.
11. Bengtsson-Palme J, Boulund F, Fick J, Kristiansson E, Larsson DGJ. Shotgun metagenomics reveals a wide array of antibiotic resistance genes and mobile elements in a polluted lake in India. Front Microbiol. 2014;5:648.
12. Gullberg E, Albrecht LM, Karlsson C, Sandegren L, Andersson DI. Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. MBio. 2014;5:e01918-14.
13. Gerdes K, Rasmussen PB, Molin S. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc Natl Acad Sci U S A. 1986;83:3116-20.
14. Acland A, Agarwala R, Barrett T, Beck J, Benson DA, Bollin C, et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 2014;42:D7.
15. Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DGJ. BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res. 2014;42:D737-43.
16. The resqu database. http://www.1928diagnostics.com/resdb/. Accessed 6 June 2014.
17. Gillespie JJ, Wattam AR, Cammer SA, Gabbard JL, Shukla MP, Dalay O, et al. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect Immun. 2011;79:4286-98.
18. Kanehisa M. The KEGG database. Novartis Found Symp. 2002;247:91-101.
19. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460-1.
20. Guglielmini J, Néron B, Abby SS, Garcillán-Barcia MP, de la Cruz F, Rocha EP. Key components of the eight classes of type IV secretion systems involved in bacterial conjugation or protein secretion. Nucleic Acids Res. 2014;42:5715-27.
21. Smillie C, Garcillán-Barcia MP, Francia MV, Rocha EP, de la Cruz F. Mobility of plasmids. Microbiol Mol Biol Rev. 2010;74:434-52.
22. Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7:e1002195.
23. Finn RD, Bateman J, Clements P, Coggill P, Eberhardt RY, Eddy SR, et al. The Pfam protein families. Nucleic Acids Res. 2014;42:D222-30.
24. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498-504.
25. R Development Core Team. R: a Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2013. http://www.r-project.org/.
26. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T,et al. gplots: Various R programming tools for plotting data. The Comprehensive Archive Network. 2011; http://cran.r-project.org/package=gplots. R package version 0.9-38.
27. Kazama H, Hamashima H, Sasatsu M, Arai T. Characterization of the antiseptic-resistance gene qacEdelta1 isolated from clinical and environmental isolates of Vibrio parahaemolyticus and Vibrio cholerae non-O1. FEMS Microbiol Lett. 1999;174:379-84.
28. Kholodii GY, Yurieva OV, Lomovskaya OL, Gorlenko Z, Mindlin SZ, Nikiforov VG. Tn5053, a mercury resistance transposon with integron's ends. J Mol Biol. 1993;230:1103-7.
29. Skurnik D, Ruimy R, Ready D, Ruppe E, Bernède-Bauduin C, Djossou F, et al. Is exposure to mercury a driving force for the carriage of antibiotic resistance genes? J Med Microbiol. 2010;59:804-7.
30. Schottel J, Mandal A, Clark D, Silver S, Hedges RW. Volatilisation of mercury and organomercurials determined by inducible R-factor systems in enteric bacteria. Nature. 1974;251:335-7.
31. Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J, et al. Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J. 2011;5:1253-61.
32. Gillings MR, Xuejun D, Hardwick SA, Holley MP, Stokes HW. Gene cassettes encoding resistance to quaternary ammonium compounds: a role in the origin of clinical class 1 integrons? ISME J. 2009;3:209-15.
33. Roseer SJ, Young HK. Identification and characterization of class 1 integrons in bacteria from an aquatic environment. J Antimicrob Chemother. 1999;44:11-8.
34. Gillings MR, Krishnan S, Worden PJ, Hardwick SA. Recovery of diverse genes for class 1 integron-integrases from environmental DNA samples. FEMS Microbiol Lett. 2008;287:56-62.
35. Gillings MR, Gaze WH, Pruden A, Smalla K, Tiedje JM, Zhu YG. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 2015;9:1269-79.
36. Hughes VM, Datta N. Conjugative plasmids in bacteria of the 'pre-antibiotic' era. Nature. 1983;302:725-6.
37. Hobman JL, Crossman L. Bacterial antimicrobial metal ion resistance. J Med Microbiol. 2014;64:471-97.
38. Castillo M, Martin-Orue SM, Taylor-Pickard JA, Pèrez JF, Gasa J. Use of mannanoligosaccharides and zinc chelate as growth promoters and diarrhea preventative in weaning pigs: Effects on microbiota and gut function. J Anim Sci. 2008;86:94-101.
39. Li YX, Xiong X, Chun-ye L, Zhang FS, Wei L, Wei H. Cadmium in animal production and its potential hazard on Beijing and Fuxin farmlands. J Hazard Mater. 2010;177:475-80.
40. Levy SB. Active efflux, a common mechanism for biocide and antibiotic resistance. Symp Ser Soc Appl Microbiol. 2002;31:65S-71S.
41. Silver S, Phung LT. Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol. 1996;50:753-89.
42. Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev. 2003;27:313-39.
43. Cavaco LM, Hasman H, Aarestrup FM. Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet Microbiol. 2011;150:344-8.
44. Amachawadi RG, Shelton NW, Shi X, Vinasco J, Dritz SS, Tokach MD, et al. Selection of fecal enterococci exhibiting tcrB-mediated copper resistance in pigs fed diets supplemented with copper. Appl Environ Microbiol. 2011;77:5597-603.
45. Sütterlin S, Edquist P, Sandegren L, Adler M, Tängdèn T, Drobni M, et al. Silver resistance genes are overrepresented among Escherichia coli isolates with CTX-M production. Appl Environ Microbiol. 2014;80:6863-9.
46. McDonnell G, Russell AD. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev. 1999;12:147-79.
47. Maillard JY. Antimicrobial biocides in the healthcare environment: efficacy, usage, policies, and perceived problems. Ther Clin Risk Manag. 2005;1:307-20.
48. Nachman KE, Baron PA, Raber G, Francesconi KA, Navas-Acien A, Love DC. Roxarsone, inorganic arsenic, and other arsenic species in chicken: a U.S.-based market basket sample. Environ Health Perspect. 2013;121:818-24.
49. Chen YT, Lauderdale TL, Liao TL, Shiau YR, Shu HY, Wu KM, et al. Sequencing and comparative genomic analysis of pK29, a 269-kilobase conjugative plasmid encoding CMY-8 and CTX-M-3 betalactamases in Klebsiella pneumoniae. Antimicrob Agents Chemother. 2007;51:3004-7.
50. Woodford N, Carattoli A, Karisik E, Underwood A, Ellington MJ, Livermore DM. Complete nucleotide sequences of plasmids pEK204, pEK499, and pEK516, encoding CTX-M enzymes in three major Escherichia coli lineages from the United Kingdom, all belonging to the international O25:H4-ST131 clone. Antimicrob Agents Chemother. 2009;53:4472-82.
51. Sandegren L, Linkevicius M, Lytsy B, MelhusÅ, Andersson DI. Transfer of an Escherichia coli ST131 multiresistance cassette has created a Klebsiella pneumoniae-specific plasmid associated with a major nosocomial outbreak. J Antimicrob Chemother. 2012;67:74-83.
52. Berg J, Tom-Petersen A, Nybroe O. Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett Appl Microbiol. 2005;40:146-51.
53. Knapp CW, McCluskey SM, Singh BK, Campbell CD, Hudson G, Graham DW. Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS One. 2011;6:e27300.
54. Seiler C, Berendonk TU. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 2012;3:399.
55. Stepanauskas R, Gless T, Jagoe C, Tuckfield RC, Lindell AH, McArthur JV. Elevated microbial tolerance to metals and antibiotics in metal-contaminated industrial environments. Environ Sci Technol. 2005;39:3671-8.
56. Hornung C, Poehlein A, Haack FS, Schmidt M, Dierking K, Pohlen A, et al. The Janthinobacterium sp. HH01 genome encodes a homologue of the V. cholerae CqsA and L. pneumophila LqsA autoinducer synthases. PLoS One. 2013;8:e55045.
57. Giovannoni SJ, Cameron TJ, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8:1553-65.
58. Yooseph S, Nealson KH, Rusch DB, McCrow JP, Dupont CL, Kim M, et al. Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature. 2010;468:60-6.
59. Mira A, Ochman H, Moran NA. Deletional bias and the evolution of bacterial genomes. Trends Genet. 2001;17:589-96.
60. Sakharkar KR, Dhar PK, Chow VT. Genome reduction in prokaryotic obligatory intracellular parasites of humans: a comparative analysis. Int J Syst Evol Microbiol. 2004;54:1937-41.
61. Bengtsson-Palme J, Rosenblad MA, Molin M, Blomberg A. Metagenomics reveals that detoxification systems are underrepresented in marine bacterial communities. BMC Genomics. 2014;15:749.
62. Egan ES, Fogel MA, Waldor MK. Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes. Mol Microbiol. 2005;56:1129-38.
63. Touchon M, Bobay LM, Rocha EP. The chromosomal accommodation and domestication of mobile genetic elements. Curr Opin Microbiol. 2014;22:22-9.
64. Shintani M, Sanchez ZK, Kimbara K. Genomics of microbial plasmids: classification and identification based on replication and transfer systems and host taxonomy. Front Microbiol. 2015;6:242.
65. McDonnell RW, Sweeney HM, Cohen S. Conjugational transfer of gentamicin resistance plasmids intraspecifically and interspecifically in Staphylococcus aureus and Staphylococcus epidermidis. Antimicrob Agents Chemother. 1983;23:151-60.
66. Randall CP, Gupta A, Jackson N, Busse D, O'Neill AJ. Silver resistance in Gram-negative bacteria: a dissection of endogenous and exogenous mechanisms. J Antimicrob Chemother. 2015;70:1037-46.
67. Hooper DC. Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis. 2001;7:337-41.
68. Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR, Schweizer HP. Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob Agents Chemother. 2001;45:428-32.