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Antibiotic Resistance is Widespread in Urban Aquatic Environments of Rio de Janeiro, Brazil

  • Microbiology of Aquatic Systems
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Abstract

Bacterial resistance to antibiotics has become a public health issue. Over the years, pathogenic organisms with resistance traits have been studied due to the threat they pose to human well-being. However, several studies raised awareness to the often disregarded importance of environmental bacteria as sources of resistance mechanisms. In this work, we analyze the diversity of antibiotic-resistant bacteria occurring in aquatic environments of the state of Rio de Janeiro, Brazil, that are subjected to distinct degrees of anthropogenic impacts. We access the diversity of aquatic bacteria capable of growing in increasing ampicillin concentrations through 16S rRNA gene libraries. This analysis is complemented by the characterization of antibiotic resistance profiles of isolates obtained from urban aquatic environments. We detect communities capable of tolerating antibiotic concentrations up to 600 times higher than the clinical levels. Among the resistant organisms are included potentially pathogenic species, some of them classified as multiresistant. Our results extend the knowledge of the diversity of antibiotic resistance among environmental microorganisms and provide evidence that the diversity of drug-resistant bacteria in aquatic habitats can be influenced by pollution.

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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

    Article  CAS  PubMed  Google Scholar 

  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 5:403–410

    Article  Google Scholar 

  3. Andersson DI, Levin BR (1999) The biological cost of antibiotic resistance. Curr Opin Microbiol 2:489–493

    Article  CAS  PubMed  Google Scholar 

  4. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Ball M, Gómez W, Magallanes X, Rosales R, Melfo A, Yarzábal L.A (2013) Bacteria recovered from high-altitude, tropical glacier in Venezuelan Andes. World J Microbol Biotechnol

  6. Baquero F, Martínez JL, Cantón R (2008) Antibiotic and antibiotic resistance in water environments. Curr Opin Biotechnol 19:260–265

    Article  CAS  PubMed  Google Scholar 

  7. Bennett PM (2008) Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 153(Suppl 1):S347–S357

    PubMed Central  CAS  PubMed  Google Scholar 

  8. Bhullar K, Waglechner N, Pawlowski A, Koteva K, Banks E.D, Johnston M.D. et al. (2012) Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE

  9. Cantón R (2009) Antibiotic resistance genes from the environment: a perspective through newly identified antibiotic resistance mechanisms in the clinical setting. Clin Microbiol Infect 15(Suppl 1):20–25

    Article  PubMed  Google Scholar 

  10. Carlet J, Jarlier V, Harbarth S, Voss A, Gossens H, Pittet D (2012) Ready for a world without antibiotics? The Pensières antibiotic resistance call to action. Antimicrob Restist Infect Control 14:11–23

    Article  Google Scholar 

  11. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261

    Article  CAS  PubMed  Google Scholar 

  12. Cole JR, Wang Q, Crdenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:141–145

    Article  Google Scholar 

  13. Czekalski N, Berthold T, Caucci S, Egli A, Bürgmann H (2012) Increased levels of multiresistant bacteria and resistance genes after wastewater treatment and their dissemination into Lake Geneva, Switzerland. Front Microbiol 3:106

    PubMed Central  PubMed  Google Scholar 

  14. D'Costa VM, Griffiths E, Wright GD (2007) Expanding the soil antibiotic resistome: exploring environmental diversity. Curr Opin Microbiol 10:481–489

    Article  PubMed  Google Scholar 

  15. Dantas G, Sommer MOA, Oluwasegun RD, Church GM (2008) Bacteria subsisting on antibiotics. Science 320:100–103

    Article  CAS  PubMed  Google Scholar 

  16. Davies J (2006) Are antibiotics naturally antibiotics? J Indust Microbiol Biotechnol 33:496–499

    Article  CAS  Google Scholar 

  17. De Souza MJ, Nair S, Loka Bharathi PA, Chandramohan D (2006) Metal and antibiotic-resistance in psychrotrophic bacteria from Antarctic Marine waters. Ecotoxicology 15:379–384

    Article  PubMed  Google Scholar 

  18. Deris JB, Kim M, Zhang Z, Okano H, Hersmen R, Groisman A, Hwa T (2013) The innate growth bistability and fitness landscapes of antibiotic-resistant bacteria. Science 342:12374351–12374358

    Article  Google Scholar 

  19. Dethlefsen, L., Huse, S, Sogin, M.L., Relman, D.A. (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biology.

  20. D’Costa VM, King CE, Kalan L, Morar M, Sung WWL, Schwarz C et al (2011) Antibiotic resistance is ancient. Nature 477:457–461

    Article  PubMed  Google Scholar 

  21. D’Costa VM, McGrann KM, Hughes DW, Wright GD (2006) Sampling the antibiotic resistome. Science 311:374–377

    Article  PubMed  Google Scholar 

  22. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Edwing B, Hillier L, Wendl M, Green P (1998) Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Gen Res 8:175–185

    Article  Google Scholar 

  24. Forbserg KJ, Reyes A, Wang B, Selleck EM, Sommer MOA, Dantas G (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337:1107–1111

    Article  Google Scholar 

  25. Gaze WH, Krone SM, Joakim-Larsson DG, Li XZ, Robinson JA, Simonet P et al (2013) Influence of humans on the evolution and mobilization of environmental antibiotic resistome. Emerg Infect Dis 19:1–7

    Article  Google Scholar 

  26. Gifford DR, MacLean RC (2013) Evolutionary reversals of antibiotic resistance in experimental populations of Pseudomonas aeruginosa. Evolution 67:2973–2981

    PubMed  Google Scholar 

  27. Gillings MR, Stokes HW (2012) Are humans increasing bacterial evolvability? Trends Ecol Evol 27:346–352

    Article  PubMed  Google Scholar 

  28. Goh E, Yim G, Tsui W, McClure J, Surette MG, Davies J (2002) Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. PNAS 99:17025–17030

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Gregoracci G.B, Nascimento J.R, Cabral A.S, Paranhos R, Valentin J.L, Thomspon, C.C, Thompson F.L (2012) Structuring of bacterioplankton diversity in a large tropical bay. PLoS ONE

  30. Höjgård S. Antibiotic resistance—why is the problem so difficult to solve? (2012) Infect Ecol Epidemol.

  31. Jernberg C, Löfmark S, Edlund C, Jansson JK (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 1:56–66

    Article  CAS  PubMed  Google Scholar 

  32. Juhas M (2013) Horizontal gene transfer in human pathogens. Crit Rev in Microbiol

  33. Kristiansson E, Fick J, Janzon A, Grabic R, Rutgersson C, Weijdegår B, Söderström H, Larsson D.G (2011) Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS ONE

  34. Kümmerer K (2009) Antibiotics in the aquatic environment—a review. Part II. Chemosphere 75:435–441

    Article  PubMed  Google Scholar 

  35. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. Wiley, New York, pp 115–175

    Google Scholar 

  36. Levy SB, Marshall B (2004) Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10(12 Suppl):122–129

    Article  Google Scholar 

  37. Linares JF, Gustafsson I, Baquero F, Martínez JL (2006) Antibiotics as intermicrobial signaling molecules instead of weapons. PNAS 103:19484–19489

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Lozupone C, Hamady M, Knight R (2006) UniFrac - an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinforma 7:371–384

    Article  Google Scholar 

  39. Lupo A, Coyne S, Berendonk TU (2012) Origin and evolution of antibiotic resistance: the commom mechanisms of emergence and spread in water bodies. Front Microbiol 3:18

    PubMed Central  PubMed  Google Scholar 

  40. Martínez JL (2008) Antibiotics and antibiotic resistance genes in natural environments. Science 321:365–367

    Article  PubMed  Google Scholar 

  41. Martínez JL (2009) Environmental pollution by antibiotics and antibiotic resistance determinants. Environ Pollut 157:2893–2902

    Article  PubMed  Google Scholar 

  42. Martínez JL (2012) Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Front Microbiol 3:1

    PubMed Central  PubMed  Google Scholar 

  43. Martínez JL, Baquero F, Andersson DI (2007) Predicting antibiotic resistance. Nat Rev Microbiol 5:958–965

  44. Pai V, Rao VI, Rao SP (2010) Prevalence and antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus [MRSA] isolates at a tertiary care hospital in Mangalore, South India. J Lab Phys 2:82–84

    Google Scholar 

  45. Pruden A, Pei R, Storteboom H, Carlson KH (2006) Antibiotic resistance genes as emerging contaminants: studies in Northern Colorado. Environ Sci Technol 40:7745–7750

    Article  Google Scholar 

  46. Santoro DO, Romão CMCA, Clementino MM (2012) Decreased aztreonam susceptibility among Pseudomonas aeruginosa isolates from hospital effluent treatment system and clinical samples. Int J Environ Health Res 22:560–570

    Article  CAS  PubMed  Google Scholar 

  47. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  48. Schwartz T, Kohnen W, Jansen B, Obst U (2003) Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water and drinking water biofilms. FEMS Microbiol Ecol 43:325–335

    Article  CAS  PubMed  Google Scholar 

  49. Segawa T, Takeuchi N, Rivera A, Yamada A, Yoshimura Y, Barcaza G et al (2013) Distribution of antibiotic resistance in glacier environments. Environ Microbiol Rep 5:127–134

    Article  CAS  PubMed  Google Scholar 

  50. Sejas LM, Silbert S, Reis AO, Sader HS (2003) Avaliação da qualidade dos discos com antimicrobianos para testes de disco-difusão disponíveis comercialmente no Brasil. Jornal Brasileiro de Patologia e Medicina Laboratorial 39:27–35

    Article  CAS  Google Scholar 

  51. Sengupta S, Chattopadhyay MK, Grossart HP (2013) The multifaceted roles of antibiotics and antibiotic resistance in nature. Front Microbiol 4:47

    PubMed Central  PubMed  Google Scholar 

  52. Silveira CB, Vieira RP, Cardoso AM, Paranhos R, Albano RM, Martins OB (2011) Influence of salinity on bacterioplankton communities from the Brazilian rain forest to the coastal Atlantic Ocean. PloS One

  53. Sommer MO, Dantas G, Church GM (2009) Functional characterizathion of the antibiotic resitance reservoir in the human microflora. Science 325:1128–1131

    Article  CAS  PubMed  Google Scholar 

  54. Tacão M, Correia A, Henriques I (2012) Resistance to broad-spectrum antibiotics in aquatic systems: anthropogenic activities modulate the dissemination of blaCTX-M-like genes. Appl Environ Microbiol 78:4134–4140

    Article  PubMed Central  PubMed  Google Scholar 

  55. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  56. Thevenon F, Adatte T, Wildi W, Poté J (2012) Antibiotic resistant bacteria/genes dissemination in lacustrine sediments highly increased following cultural eutrophication of Lake Geneva (Switzerland). Chemosphere 86:468–476

    Article  CAS  PubMed  Google Scholar 

  57. Vieira RP, Gonzalez AM, Cardoso AM, Oliveira DN, Albano RM, Clementino MM, Martins OB, Paranhos R (2008) Relationships between bacterial diversity and environmental variables in a tropical marine environment, Rio de Janeiro. Environ Microbiol 10:189–199

    CAS  PubMed  Google Scholar 

  58. Vieira RP, Clementino MM, Cardoso AM, Oliveira DN, Albano RM, Gonzalez AM et al (2007) Archaeal Communities in a Tropical Estuarine Ecosystem: Guanabara Bay, Brazil. Microb Ecol 54:460–462

    Article  PubMed  Google Scholar 

  59. Vignesh S, Muthukumar K, James RA (2012) (2012) Antibiotic resistant pathogens versus human impacts: a study from three eco-regions of the Chennai coast, southern India. Mar Pollut Bull 64:790–800

    Article  CAS  PubMed  Google Scholar 

  60. Walsh F (2013) Investigating antibiotic resistance in non-clinical environments. Front Microbiol 4:19

    PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  62. Wise R (2002) Antimicrobial resistance: priorities for action. J Antimicrob Chemother 49:585–586

    Article  CAS  PubMed  Google Scholar 

  63. World Health Organization (WHO) (2000) WHO Annual report on infectious disease: overcoming antimicrobial resistance. World Health Organization: Geneva, Switzerland, 2000. http://www.who.int/infectious-disease-report/2000/

  64. World Health Organization (WHO) (2012) Fact sheet N°194: antimicrobial resistance. http://www.who.int/mediacentre/factsheets/fs194/en/index.html

  65. Wright GD (2007) The antibiotic resistome: the nexus of chemical genetic diversity. Nat Rev Microbiol 5:175–186

    Article  CAS  PubMed  Google Scholar 

  66. Wright GD (2010) Antibiotic resistance in the environment: a link to the clinic? Curr Opin Microbiol 13:589–594

    Article  CAS  PubMed  Google Scholar 

  67. Yim G, Wang H, Davies J (2007) Antibiotics as signaling molecules. Philos Trans R Soc Lond B Biol Sci 362:1195–1200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  68. Zhang Q, Lambert G, Liao D, Kim H, Robin K, Tung CK et al (2011) Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333:1764–1767

    Article  CAS  PubMed  Google Scholar 

  69. Zhang XX, Zhang T, Fang HH (2009) Antibiotic resistance genes in water environment. Appl Microbiol Biotechnol 82:397–414

    Article  CAS  PubMed  Google Scholar 

  70. Salloto GRB, Cardoso AM, Coutinho FH, Pinto LH, Vieira RP, Chaia C, Lima JL et al (2012) Pollution impacts on bacterioplankton diversity in a tropical urban coastal lagoon system. PLoS ONE 7(11):e51175

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  71. Singh GB (2004) β-Lactams in the new millennium. Part I: monobactams and carbapenems. Mini Rev Med Chem 4:69–92

    Article  CAS  PubMed  Google Scholar 

  72. Rajpara N, Patel A, Tiwari N, Bahuguna J, Antony A, Choudhury I et al (2009) Int J Antimicrob Agents 34(3):220–225

    Article  CAS  PubMed  Google Scholar 

  73. Ahmed AM, Nakagawa T, Arakawa E, Ramamurthy T, Shinoda S, Shimamoto T (2004) New aminoglycoside acetyltransferase gene, aac(3)-Id, in a class 1 integron from a multiresistant strain of Vibrio fluvialis isolated from an infant aged 6 months. J Antimicrob Chemother 53(6):947–951

    Article  CAS  PubMed  Google Scholar 

  74. Bonomo RA, Szabo D (2006) Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin Infect Dis 43:S49–S56

    Article  CAS  PubMed  Google Scholar 

  75. Quinteira S, Ferreira H, Peixe L (2005) First Isolation of blaVIM-2 in an environmental isolate of Pseudomonas pseudoalcaligenes. Antimicrob Agents Chemother 49(5):2140–2141

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  76. Tremaroli V, Fedi S, Turner RJ, Ceri H, Zannoni D (2008) Pseudomonas pseudoalcaligenes KF707 upon bioWlm formation on a polystyrene surface acquire a strong antibiotic resistance with minor changes in their tolerance to metal cations and metalloid oxyanions. Arch Microbiol 190(1):29–39

    Article  CAS  PubMed  Google Scholar 

  77. Nazl SA, Tariq P (2005) Prevalence and antibiogram pattern of Pseudomonas species causing secondary infectious among patients of pulomnary tuberculosis. Int Chem Pharm Med J 2(2):231–237

    Google Scholar 

  78. Rice LB (2009) The clinical consequences of antimicrobial resistance. Curr Opin Microbiol 12(5):476–481

    Article  CAS  PubMed  Google Scholar 

  79. Depardieu F, Podglajen I, Leclercq R, Collatz E, Courvalin P (2007) Modes and modulation of antibiotic resistance gene expression. Clin Microbiol Rev 20(1):79–114

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was financed by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ). We acknowledge genome studies facilities Johanna Döbereiner. Special thanks to Joyce Lemos Lima for preparing sequencing reactions.

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Authors and Affiliations

  1. Instituto de Bioquímica Médica, Universidade Federal do Rio de Janeiro, UFRJ, Rio de Janeiro, Brazil

    Felipe H. Coutinho, Leonardo H. Pinto, Orlando B. Martins & Ricardo P. Vieira

  2. Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, UFRJ, Rio de Janeiro, Brazil

    Felipe H. Coutinho & Cynthia B. Silveira

  3. Instituto Nacional de Controle de Qualidade em Saúde, FIOCRUZ, Rio de Janeiro, Brazil

    Gigliola R. B. Salloto, Ricardo P. Vieira & Maysa M. Clementino

  4. Centro Universitário Estadual da Zona Oeste, UEZO, Rio de Janeiro, Brazil

    Alexander M. Cardoso

  5. Laboratório de Microbiologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, CCS—21941-590, Ilha do Fundão, P.O. Box 68011, 21944-970, Rio de Janeiro, RJ, Brazil

    Felipe H. Coutinho

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  1. Felipe H. Coutinho
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  2. Cynthia B. Silveira
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  7. Ricardo P. Vieira
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  8. Maysa M. Clementino
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Coutinho, F.H., Silveira, C.B., Pinto, L.H. et al. Antibiotic Resistance is Widespread in Urban Aquatic Environments of Rio de Janeiro, Brazil. Microb Ecol 68, 441–452 (2014). https://doi.org/10.1007/s00248-014-0422-5

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