Sources of antibiotics in natural environments and their biological role

COMMENTARY ON THE LAW

Sources of antibiotics in natural environments and their biological role

Agnieszka Zabłotni 1 , Adam Jaworski 2

1. Zakład Mikrobiologii Ogólnej, Wydział Biologii i Ochrony Środowiska, Uniwersytet Łódzki
2. Zakład Genetyki Drobnoustrojów, Wydział Biologii i Ochrony Środowiska, Uniwersytet Łódzki, obecne miejsce pracy: Społeczna Akademia Nauk w Łodzi

Published: 2014-08-29
DOI: 10.5604/17322693.1119027
GICID: 01.3001.0003.1279
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2014; 68 : 1040-1049

 

Abstract

Nowadays antibiotics are broadly used not only for treatment of bacterial infections but also in nonmedical applications. For many years they have been added as livestock and poultry growth supplements, and they are applied similarly in fish farming. In basically unchanged form they may get into the natural environment and remain there for a long time. Excessive use of antibiotics leads to widespread of antibiotic resistance among clinical and environmental bacterial strains. Subinhibitory concentrations of antibiotics, which do not inhibit growth of bacteria, are often found in soil, water or even in the tissue of different organisms. Such low concentrations affect many bacterial genes through changes in their transcription level and increase of the mutation rate, and as a consequence lead to many bacterial adaptations to environmental stresses. There is also evidence that subinhibitory concentrations of antibiotics induce transfer of mobile genetic elements through horizontal gene transfer pathways, and therefore enhance antibiotic resistance, also among environmental strains. The analyzed data suggest the necessity of restriction and regular monitoring of antibiotics, which may be considered as environmental pollutants.

References

  • 1. Aarestrup F.M.: Sustainable farming: get pigs of antibiotics. Nature,2012; 486: 465-466
    Google Scholar
  • 2. Aertsen A., Michiels C.W.: Mrr instigates the SOS response afterhigh pressure stress in Escherichia coli. Mol. Microbiol., 2005; 58:1381-1391
    Google Scholar
  • 3. Aertsen A., Michiels C.W.: Upstream of the SOS response: figureout the trigger. Trends Microbiol., 2006; 14: 421-423
    Google Scholar
  • 4. Allen H.K., Donato J., Wang H.H., Cloud-Hansen K.A., Davies J.,Handelsman J.: Call of the wild antibiotic resistance genes in naturalenvironments. Nat. Rev. Microbiol., 2010; 8: 251- 259
    Google Scholar
  • 5. Allen H.K., Levine U.Y., Looft T., Bandrick M., Casey T.A.: Treatment,promotion, commotion: antibiotic alternatives in food-producinganimals. Trends. Microbiol., 2013; 21: 114-119
    Google Scholar
  • 6. Amundsen S.K, Taylor A.F., Smith G.R.: The RecD subunit of theEscherichia coli RecBCD enzyme inhibits RecA loading, homologousrecombination, and DNA repair. Proc. Natl. Acad. Sci. USA, 2000;97: 7399-7404
    Google Scholar
  • 7. Andersson D.J., Hughes D.: Antibiotic resistance and its cost: is itpossible to reverse resistance? Nat. Rev. Microbiol., 2010; 8: 260-271
    Google Scholar
  • 8. Bagge N., Schuster M., Hentzer M., Ciofu O., Givskov M., GreenbergE.P., Høiby N.: Pseudomonas aeruginosa biofilms exposed toimipenem exhibit changes in global gene expression and beta-lactamaseand alginate production. Antimicrob. Agents Chemother.,2004; 48: 1175-1187
    Google Scholar
  • 9. Baltz R.H.: Renaissance in antibacterial discovery from actinomycetes.Curr. Opin. Pharmacol., 2008; 8: 557-563
    Google Scholar
  • 10. Bartelt-Hunt S., Snow D.D., Damon-Powell T., Miesbach D.: Occurrenceof steroid hormones and antibiotics in shallow groundwaterimpacted by livestock waste control facilities. J. Contam. Hydrol.,2011; 123: 94-103
    Google Scholar
  • 11. Beaber J.W., Hochhut B., Waldor M.K.: SOS response promoteshorizontal dissemination of antibiotic resistance genes. Nature,2004; 427: 72-74
    Google Scholar
  • 12. Berdy J.: Bioactive microbial metabolites. J. Antibiot., 2005; 58:1-26
    Google Scholar
  • 13. Bielaszewska M., Idelevich E.A., Zhang W., Bauwens A., SchaumburgF., Mellmann A., Peters G., Karch H.: Effects of antibiotics onShiga toxin 2 production and bacteriophage induction by epidemicEscherichia coli O104:H4 strain. Antimicrob. Agents Chemother.,2012; 56: 3277-3282
    Google Scholar
  • 14. Blázquez J., Couce A., Rodríguez-Beltrán J., Rodríguez-Rojas A.:Antimicrobials as promoters of genetic variation. Curr. Opin. Microbiol.,2012; 15: 561-569
    Google Scholar
  • 15. Brazas M.D., Hancock R.E.: Using microarray gene signaturesto elucidate mechanisms of antibiotic action and resistance. DrugDiscov. Today, 2005; 10: 1245-1252
    Google Scholar
  • 16. Bruchmann J., Kirchen S., Schwartz T.: Sub-inhibitory concentrationsof antibiotics and wastewater influencing biofilm formationand gene expression of multi-resistant Pseudomonas aeruginosa wastewaterisolates. Environ. Sci. Pollut. Res. Int., 2013; 20: 3539-3549
    Google Scholar
  • 17. Cabello F.C., Godfrey H.P., Tomova A., Ivanova L., Dölz H., MillanaoA., Buschmann A.H.: Antimicrobial use in aquaculture re-examined:its relevance to antimicrobial resistance and to animal andhuman health. Environ. Microbiol., 2013; 15: 1917-1942
    Google Scholar
  • 18. Cairns J., Foster P.L. Adaptive reversion of a frameshift mutationin Escherichia coli. Genetics, 1991; 128: 695-701
    Google Scholar
  • 19. Canton R.: Antibiotic resistance genes from the environment:a perspective through newly identified antibiotic resistance mechanismsin the clinical setting. Clin. Microbiol. Infect., 2009; 15, Suppl.1:20-25
    Google Scholar
  • 20. Cattoir V., Poirel L., Aubert C., Soussy C.J.: Unexpected occurrenceof plasmid-mediated quinolone resistance determinants inenvironmental Aeromonas spp. Emerg. Infect. Dis., 2008; 14: 231-237
    Google Scholar
  • 21. Chiang S.M., Schellhorn H.E.: Evolution of the RpoS regulon:origin of RpoS and the conservation of RpoS-dependent regulationin bacteria. J. Mol. Evol., 2010; 70: 557-571
    Google Scholar
  • 22. Couce A., Blazquez J.: Side effects of antibiotics on genetic variability.FEMS Microbiol. Rev., 2009; 33: 531-538
    Google Scholar
  • 23. Courcelle J., Khodursky A., Peter B., Brown P.O., Hanawalt P.C.:Comparative gene expression profiles following UV exposure inwild-type and SOS-deficient Escherichia coli. Genetics, 2001; 158: 41-64
    Google Scholar
  • 24. Cromwell G.L.: Why and how antibiotics are used in swine production.Anim. Biotechnol., 2002; 13: 7-27
    Google Scholar
  • 25. Dantas G., Sommer M.O., Oluwasegun R.D., Church G.M.: Bacteriasubsisting on antibiotics. Science, 2008; 320: 100-103
    Google Scholar
  • 26. Darwish W.S., Eldaly E.A., El-Abbasy M.T., Ikenaka Y., NakayamaS., Ishizuka M.: Antibiotic residues in food: the African scenario. Jpn.J. Vet. Res., 2013; 61, Suppl.: S13-S22
    Google Scholar
  • 27. Davies J.: Small molecules: the lexicon of biodiversity. J. Biotechnol.,2007; 129: 3-5
    Google Scholar
  • 28. Davies J., Ryan K.S.: Introducing the parvome: bioactive compoundsin the microbial word. ACS Chem. Biol., 2012; 7: 252-259
    Google Scholar
  • 29. Davies J., Spiegelman G.B., Yim G.: The world of subinhibotoryconcentrations. Curr. Opin. Microbiol., 2006; 9: 445-453
    Google Scholar
  • 30. D’Costa V.M., McGrann K.M., Hughes D.W., Wright G.D.: Samplingthe antibiotic resistome. Science, 2006; 311: 374-377
    Google Scholar
  • 31. Dibner J.J., Richards J.D.: Antibiotic growth promoters in agriculture:history and mode of action. Poultry Sci., 2005; 84: 634-643
    Google Scholar
  • 32. Eltayb A., Barakat S., Marrone G., Shaddad S., Stålsby LundborgC.: Antibiotic use and resistance in animal farming: a quantitativeand qualitative study on knowledge and practices among farmers inKhartoum, Sudan. Zoonoses Public Health, 2012; 59: 330-338
    Google Scholar
  • 33. Galan J.C., González-Candelas F., Rolain J.M., Cantón R.: Antibioticsas selectors and accelerators of diversity in the mechanismsof resistance: from the resistome to genetic plasticity in theβ-lactamases world. Front. Microbiol., 2013; 4: 9
    Google Scholar
  • 34. Gebreyohannes G., Moges F., Sahile S., Raja N., Reetha D.: Isolationand characterization of potential antibiotic producing actinomycetesfrom water and sediments of Lake Tana, Ethiopia. AsianPac. J. Trop. Biomed., 2013; 3: 426-435
    Google Scholar
  • 35. Gillespie S.H., Basu S., Dickens A.L., O’Sullivan D.M., McHughT.D.: Effect of subinhibitory concentrations of ciprofloxacin on Mycobacteriumfortuitum mutation rates. J. Antimicrob. Chemother.,2005; 56: 344-348
    Google Scholar
  • 36. Gillings M.R.: Evolutionary consequences of antibiotic use forthe resistome, mobilome, and microbial pangenome. Front. Microbiol.,2013; 4: 4
    Google Scholar
  • 37. Goh E.B., Yim G., Tsui W., McClure J., Surette M.G., Davies J.:Transcriptional modulation of bacterial gene expression by subinhibitoryconcentrations of antibiotics. Proc. Natl. Acad. Sci. USA.,2002; 99: 17025-17030
    Google Scholar
  • 38. Grimwood K., To M., Rabin H.R., Woods D.E.: Inhibition of Pseudomonasaeruginosa exoenzyme expression by subinhibitory antibioticconcentrations. Antimicrob. Agents Chemother., 1989; 33: 41-47
    Google Scholar
  • 39. Gutierrez A., Laureti L., Crussard S., Abida H., Rodriguez-RojasA., Blazquez J., Baharoglu Z., Mazel D., Darfeuille F., Vogel J., Matic I.:β-lactam antibiotics promote bacterial mutagenesis via an RpoS-mediatedreduction in replication fidelity. Nat. Commun., 2013; 4: 1610
    Google Scholar
  • 40. Hastings P.J., Rosenberg S.M., Slack A.: Antibiotic-induced lateraltransfer of antibiotic resistance. Trends Microbiol., 2004; 12: 401-404
    Google Scholar
  • 41. Henderson-Begg S.K., Livermore D.M., Hall L.M.: Effect of subinhibitoryconcentrations of antibiotics on mutation frequency inStreptococcus pneumoniae. J. Antimicrob. Chemother., 2006; 57: 849-854
    Google Scholar
  • 42. Hengge-Aronis R.: Signal transduction and regulatory mechanismsinvolved in control of the δS (RpoS) subunit of RNA polymerase.Microbiol. Mol. Biol. Rev., 2002; 66: 373-395
    Google Scholar
  • 43. Hoiby N.: Ecological antibiotic policy. J. Antimicrob. Chemother.,2000; 46, Suppl. A: 59-62
    Google Scholar
  • 44. Hryniewicz W.: Antybiotykooporność – co musimy zrobić dziś?Pol. Merkuriusz Lek., 2011; 30: 305-309
    Google Scholar
  • 45. Joo H.S., Chan J.L., Cheung G.Y., Otto M.: Subinhibitory concentrationsof protein synthesis-inhibiting antibiotics promote increasedexpression of the agr virulence regulator and production ofphenol-soluble modulin cytolysins in community-associated methicillin-resistantStaphylococcus aureus. Antimicrob. Agents Chemother.,2010; 54: 4942-4944
    Google Scholar
  • 46. Kai T., Tateda K., Kimura S., Ishii Y., Ito H., Yoshida H., KimuraT., Yamaguchi K.: A low concentration of azithromycin inhibits themRNA expression of N-acyl homoserine lactone synthesis enzymes,upstream of lasI or rhlI, in Pseudomonas aeruginosa. Pulm. PharmacolTher., 2009; 22: 483-486
    Google Scholar
  • 47. Kaplan J.B., Izano E.A., Gopal P., Karwacki M.T., Kim S., Bose J.L.,Bayles K.W., Horswill A.R.: Low levels of β-lactam antibiotics induceextracellular DNA release and biofilm formation in Staphylococcusaureus. mBio., 2012; 3: e00198-e00212
    Google Scholar
  • 48. Kohanski M.A., DePristo M.A., Collins J.J.: Sublethal antibiotictreatment leads to multidrug resistance via radical-induced mutagenesis.Mol. Cell., 2010; 37: 311-320
    Google Scholar
  • 49. Kümmerer K.: Significance of antibiotics in the environment. J.Antimicrob. Chemother., 2003; 52: 5-7
    Google Scholar
  • 50. Kümmerer K.: Resistance in the environment. J. Antimicrob.Chemother., 2004; 54: 311-320
    Google Scholar
  • 51. Kwon J.W.: Mobility of veterinary drugs in soil with applicationof manure compost. Bull. Environ. Contam. Toxicol., 2011; 87: 40-44
    Google Scholar
  • 52. Labella A., Gennari M., Ghidini V., Trento I., Manfrin A., BorregoJ.J., Lleo M.M.: High incidence of antibiotic multi-resistant bacteriain coastal areas dedicated to fish farming. Mar. Pollut. Bull.,2013; 70: 197-203
    Google Scholar
  • 53. Laganà P., Caruso G., Minutoli E., Zaccone R., Santi D.: Susceptibilityto antibiotics of Vibrio spp. and Photobacterium damsela ssp.piscicida strains isolated from Italian aquaculture farms. New. Microbiol.,2011; 34: 53-63
    Google Scholar
  • 54. Laureti L., Matic I., Gutierrez A.: Bacterial responses and genomeinstability induced by subinhibitory concentrations of antibiotics.Antibiotics, 2013; 2: 100-114
    Google Scholar
  • 55. Layton J.C., Foster P.L.: Error-prone DNA polymerase IV is regulatedby the heat shock chaperone GroE in Escherichia coli. J. Bacteriol.,2005; 187: 449-457
    Google Scholar
  • 56. Li D., Renzoni A., Estoppey T., Bisognano C., Francois P., KelleyW.L., Lew D.P., Schrenzel J., Vaudaux P.: Induction of fibronectin adhesinsin quinolone-resistant Staphylococcus aureus by subinhibitorylevels of ciprofloxacin or by sigma B transcription factor activity ismediated by two separate pathways. Antimicrob. Agents Chemother.,2005; 49: 916-924
    Google Scholar
  • 57. Linares J.F., Gustafsson I., Baquero F., Martinez J.L.: Antibioticsas intermicrobial signaling agents instead of weapons. Proc. Natl.Acad. Sci. USA, 2006; 103: 19484-19489
    Google Scholar
  • 58. Long J.E., Renzette N., Centore R.C., Sandler S.J.: Differentialrequirements of two recA mutants for constitutive SOS expressionin Escherichia coli K-12. PLoS One, 2008; 3: e4100
    Google Scholar
  • 59. López E., Blázquez J.: Effect of subinhibitory concentrationsof antibiotics on intrachromosomal homologous recombination inEscherichia coli. Antimicrob. Agents. Chemother., 2009; 53: 3411-3415
    Google Scholar
  • 60. Łoś J.M., Łoś M., Węgrzyn A., Węgrzyn G.: Altruism of Shiga toxin-producingEscherichia coli: recent hypothesis versus experimentalresults. Front. Cell Infect. Microbiol., 2013; 2: 166
    Google Scholar
  • 61. Łoś J.M., Węgrzyn G.: Enterokrwotoczne szczepy Escherichiacoli (EHEC) i bakteriofagi kodujące toksyny Shiga. Post. Microbiol.,2011; 50: 175-190
    Google Scholar
  • 62. Makowski A., Sobczak A., Wcisło D., Adamek E., Baran W., NocońW.: Fotokatalityczna degradacja ampicyliny w roztworach wodnych.Proceedings of ECOpole, 2009; 3: 81-86
    Google Scholar
  • 63. Marr A.K., Overhage J., Bains M., Hancock R.E.: The Lon proteaseof Pseudomonas aeruginosa is induced by aminoglycosides andis involved in biofilm formation and motility. Microbiology, 2007;153: 474-482
    Google Scholar
  • 64. Marshall B.M., Ochieng D.J., Levy S.B.: Commensals: underappreciatedreservoir of antibiotic resistance. Microbe, 2009; 4: 231-238
    Google Scholar
  • 65. Martinez J.L.: Antibiotics and antibiotic resistance genes in naturalenvironments. Science, 2008; 321: 365-367
    Google Scholar
  • 66. Martinez J.L.: Environmental pollution by antibiotics and by antibioticresistance determinants. Environ. Pollut., 2009; 157: 2893-2902
    Google Scholar
  • 67. Mathew A.G., Cissell R., Liamthong S.: Antibiotic resistance inbacteria associated with food animals: a United States perspectiveof livestock production. Foodborne Pathog. Dis., 2007; 4: 115-133
    Google Scholar
  • 68. McManus P.S., Stockwell V.O., Sundin G.W., Jones A.L.: Antibioticuse in plant agriculture. Annu. Rev. Phytopathol., 2002; 40: 443-465
    Google Scholar
  • 69. Miller C., Thomsen L.E., Gaggero C., Mosseri R., Ingmer H., CohenS.N.: SOS response induction by β-lactams and bacterial defenseagainst antibiotic lethality. Science, 2004; 305: 1629-1631
    Google Scholar
  • 70. Nagel M., Reuter T., Jansen A., Szekat C., Bierbaum G.: Influenceof ciprofloxacin and vancomycin on mutation rate and transpositionof IS256 in Staphylococcus aureus. Int. J. Med. Microbiol., 2011;301: 229-236
    Google Scholar
  • 71. Nikaido H.: Multidrug resistance in bacteria. Annu. Rev. Biochem.,2009; 78: 119-146
    Google Scholar
  • 72. Pelaez F.: The historical delivery of antibiotics from microbialnatural products – can history repeat? Biochem. Pharmac., 2006;71: 981-990
    Google Scholar
  • 73. Pereira J.H., Reis A.C., Queirós D., Nunes O.C., Borges M.T., VilarV.J., Boaventura R.A.: Insights into solar TiO2-assisted photocatalyticoxidation of two antibiotics employed in aquatic animal production, oxolinic acid and oxytetracycline. Sci. Total Environ.,2013; 463-464: 274-283
    Google Scholar
  • 74. Pérez-Capilla T., Baquero M.R., Gómez-Gómez J.M., Ionel A., MartínS., Blázquez J.: SOS-independent induction of dinB transcriptionby β-lactam-mediated inhibition of cell wall synthesis in Escherichiacoli. J. Bacteriol., 2005; 187: 1515-1518
    Google Scholar
  • 75. Procópio R.E., Silva I.R., Martins M.K., Azevedo J.L., Araújo J.M.:Antibiotics produced by Streptomyces. Braz. J. Infect. Dis., 2012; 16:466-471
    Google Scholar
  • 76. Przeniosło-Siwczyńska M., Kwiatek K.: Dlaczego zakazano stosowaniaw żywieniu zwierząt antybiotykowych stymulatorów wzrostu?Życie Wet., 2013; 8: 104-108
    Google Scholar
  • 77. Rogers P.D., Liu T.T., Barker K.S., Hilliard G.M., English B.K.,Thornton J., Swiatlo E., McDaniel L.S.: Gene expression profiling ofthe response of Streptococcus pneumoniae to penicillin. J. Antimicrob.Chemother., 2007; 59: 616-626
    Google Scholar
  • 78. Schmieder R., Edwards R.: Insights into antibiotic resistancethrough metagenomic approaches. Future Microbiol., 2012; 7: 73-89
    Google Scholar
  • 79. Shaw K.J., Miller N., Liu X., Lerner D., Wan J., Bittner A., MorrowB.J.: Comparison of the changes in global gene expression ofEscherichia coli induced by four bactericidal agents. J. Mol. Microbiol.Biotechnol., 2003; 5: 105-122
    Google Scholar
  • 80. Slack A., Thornton P.C., Magner D.B., Rosenberg S.M., HastingsP.J.: On the mechanism of gene amplification induced under stressin Escherichia coli. PLoS Genet., 2006; 2: e48
    Google Scholar
  • 81. Subrt N., Mesak L.R., Davies J.: Modulation of virulence geneexpression by cell wall active antibiotics in Staphylococcus aureus. J.Antimicrob. Chemother., 2011; 66: 979-984
    Google Scholar
  • 82. Taddei F., Matic I., Radman M.: cAMP-dependent SOS inductionand mutagenesis in resting bacterial populations. Proc. Natl. Acad.Sci. USA, 1995; 92: 11736-11740
    Google Scholar
  • 83. Tanimoto K., Tomita H., Fujimoto S., Okuzumi K., Ike Y.: Fluoroquinoloneenhances the mutation frequency for meropenemselectedcarbapenem resistance in Pseudomonas aeruginosa, but useof the high-potency drug doripenem inhibits mutant formation.Antimicrob. Agents. Chemother., 2008; 52: 3795-3800
    Google Scholar
  • 84. Tsui W.H., Yim G., Wang H.H., McClure J.E., Surette M.G., DaviesJ.: Dual effects of MLS antibiotics: transcriptional modulationand interactions on the ribosome. Chem. Biol., 2004; 11: 1307-1316
    Google Scholar
  • 85. Turiel E., Bordin G., Rodríguez A.R.: Study of the evolution anddegradation products of ciprofloxacin and oxolinic acid in riverwater samples by HPLC-UV/MS/MS-MS. J. Environ. Monit., 2005;7: 189-195
    Google Scholar
  • 86. Ubeda C., Maiques E., Knecht E., Lasa I., Novick R.P., Penadés J.R.:Antibiotic-induced SOS response promotes horizontal disseminationof pathogenicity island-encoded virulence factors in staphylococci.Mol. Microbiol., 2005; 56: 836-844
    Google Scholar
  • 87. Valli S., Suvathi S.S., Aysha O., Nirmala P., Vinoth K.P., ReenaA.: Antimicrobial potential of Actinomycetes species isolated frommarine environment. Asian Pac. J. Trop. Biomed., 2012; 2: 469-473
    Google Scholar
  • 88. Vázquez M.M., Vázquez P.P., Galera M.M., García M.D.: Determinationof eight fluoroquinolones in groundwater samples with ultrasound-assistedionic liquid dispersive liquid-liquid microextractionprior to high-performance liquid chromatography and fluorescencedetection. Anal. Chim. Acta, 2012; 748: 20-27
    Google Scholar
  • 89. Ventura M., Canchaya C., Tauch A., Chandra G., Fitzgerald G.F.,Chater K.F., van Sinderen D.: Genomics of Actinobacteria: tracing theevolutionary history of an ancient phylum. Microbiol. Mol. Biol.Rev., 2007; 71: 495-548
    Google Scholar
  • 90. Wang P., Zhang X., Wang L., Zhen Z., Tang M., Li J.: Subinhibitoryconcentrations of ciprofloxacin induce SOS response and mutationsof antibiotic resistance in bacteria. Ann. Microbiol., 2010; 60: 511-517
    Google Scholar
  • 91. Yim G., Wang H.H., Davies J.: The truth about antibiotics. Int. J.Med. Microbiol., 2006; 296: 163-170
    Google Scholar
  • 92. Yim G., Wang H.H., Davies J.: Antibiotics as signalling molecules.Philos. Trans. R. Soc. B., 2007; 362: 1195-1200
    Google Scholar
  • 93. Zhuang X., Gao J., Ma A., Fu S., Zhuang G.: Bioactive moleculesin soil ecosystems: masters of the underground. Int. J. Mol. Sci.,2013; 14: 8841-8868
    Google Scholar

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