The role of biofilms as environmental reservoirs of antibiotic resistance

Frontiers in Microbiology

Volumn 6, Issue OCT, 2015, Pages

  Balcázar, José L ^a   Subirats, Jéssica ^a   Borrego, Carles M ^a,b  

^a CATALAN INSTITUTE FOR WATER RESEARCH ICRA   (Spain)

^b UNIVERSITY OF GIRONA   (Spain)

Author keywords

Antibiotic resistance genes; Aquatic ecosystems; Aquatic resistome; Biofilms; Mobile genetic elements

Indexed keywords

ANTIBIOTIC RESISTANCE; ANTIBIOTIC RESISTANCE GENE; BACTERIAL GENE; BIOFILM; CHEMICAL STRESS; CONFOCAL LASER MICROSCOPY; HORIZONTAL GENE TRANSFER; METAGENOMICS; MICROBIAL COMMUNITY; NONHUMAN; PLASMID; REVIEW; TRANSPOSON;

EID: 84946824500     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.01216     Document Type: Review

References (85)

1. Allen, H. K., Donato, J., Wang, H. H., Cloud-Hansen, K. A., Davies, J., and Handelsman, J. (2010). Call of the wild: antibiotic resistance genes in natural environments. Nat. Rev. Microbiol. 8, 251-259. doi: 10.1038/nrmicro2312
2. Anderl, J. N., Franklin, M. J., and Stewart, P. S. (2000). Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44, 1818-1824. doi: 10.1128/AAC.44.7.1818-1824.2000
3. Andersson, D. I., and Hughes, D. (2014). Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol. 12, 465-478. doi: 10.1038/nrmicro3270
4. Bagge, N., Schuster, M., Hentzer, M., Ciofu, O., Givskov, M., Greenberg, E. P., et al. (2004). Pseudomonas aeruginosa biofilms exposed to imipenem exhibit changes in global gene expression and β-lactamase and alginate production. Antimicrob. Agents Chemother. 48, 1175-1187. doi: 10.1128/AAC.48.4.1175-1187.2004
5. Baquero, F., Martínez, J.-L., and Cantón, R. (2008). Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotechnol. 19, 260-265. doi: 10.1016/j.copbio.2008.05.006
6. Battin, T. J., Sloan, W. T., Kjelleberg, S., Daims, H., Head, I. M., Curtis, T. P., et al. (2007). Microbial landscapes: new paths to biofilm research. Nat. Rev. Microbiol. 5, 76-81. doi: 10.1038/nrmicro1556
7. Beaber, J. W., Hochhut, B., and Waldor, M. K. (2004). SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427, 72-74. doi: 10.1038/nature02241
8. Bernier, S. P., and Surette, M. G. (2013). Concentration-dependent activity of antibiotics in natural environments. Front. Microbiol. 4:20. doi: 10.3389/fmicb.2013.00020
9. Bonnineau, C., Guasch, H., Proia, L., Ricart, M., Geiszinger, A., Romaní, A. M., et al. (2010). Fluvial biofilms: a pertinent tool to assess β-blockers toxicity. Aquat. Toxicol. 96, 225-233. doi: 10.1016/j.aquatox.2009.10.024
10. Börjesson, S., Dienues, O., Jarnheimer, P. A., Olsen, B., Matussek, A., and Lindgren, P. E. (2009). Quantification of genes encoding resistance to aminoglycosides, β-lactams and tetracyclines in wastewater environments by real-time PCR. Int. J. Environ. Health Res. 19, 219-230. doi: 10.1080/09603120802449593
11. Boxall, A. B. (2014). The environmental side effects of medication. EMBO Rep. 5, 1110-1116. doi: 10.1038/sj.embor.7400307
12. Brazelton, W. J., and Baross, J. A. (2009). Abundant transposases encoded by the metagenome of a hydrothermal chimney biofilm. ISME J. 3, 1420-1424. doi: 10.1038/ismej.2009.79
13. Buchfink, B., Xie, C., and Huson, D. H. (2015). Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59-60. doi: 10.1038/nmeth.3176
14. Burns, A., and Ryder, D. S. (2001). Potential for biofilms as biological indicators in Australian riverine systems. Ecol. Manag. Restor. 2, 53-64. doi: 10.1046/j.1442-8903.2001.00069.x
15. Chow, L., Waldron, L., and Gillings, M. R. (2015). Potential impacts of aquatic pollutants: sub-clinical antibiotic concentrations induce genome changes and promote antibiotic resistance. Front. Microbiol. 6:803. doi: 10.3389/fmicb.2015.00803
16. Cockerill, F. R. III. (1999). Genetic methods for assessing antimicrobial resistance. Antimicrob. Agents Chemother. 43, 199-212.
17. Costerton, J. W., Geesey, G. G., and Cheng, K. J. (1978). How bacteria stick. Sci. Am. 238, 86-95. doi: 10.1038/scientificamerican0178-86
18. Davies, J. (2006). Are antibiotics naturally antibiotics? J. Ind. Microbiol. Biotechnol. 33, 496-499. doi: 10.1007/s10295-006-0112-5
19. Davies, J., and Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74, 417-433. doi: 10.1128/MMBR.00016-10
20. Davies, J., Spiegelman, G. B., and Yim, G. (2006). The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9, 445-453. doi: 10.1016/j.mib.2006.08.006
21. Dionisio, F., Matic, I., Radman, M., Rodrigues, O. R., and Taddei, F. (2002). Plasmids spread very fast in heterogeneous bacterial communities. Genetics 162, 1525-1532.
22. Donlan, R. M. (2002). Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8, 881-890. doi: 10.3201/eid0809.020063
23. Donlan, R. M., and Costerton, J. W. (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15, 167-193. doi: 10.1128/CMR.15.2.167-193.2002
24. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461
25. Ehlers, L. J., and Bouwer, E. J. (1999). Rp4 plasmid transfer among species of Pseudomonas in a biofilm reactor. Water Sci. Technol. 39, 163-171. doi: 10.1016/S0273-1223(99)00164-X
26. Engemann, C. A., Adams, L., Knapp, C. W., and Graham, D. W. (2006). Disappearance of oxytetracycline resistance genes in aquatic systems. FEMS Microbiol. Lett. 263, 176-182. doi: 10.1111/j.1574-6968.2006.00419.x
27. Engemann, C. A., Keen, P. L., Knapp, C. W., Hall, K. J., and Graham, D. W. (2008). Fate of tetracycline resistance genes in aquatic systems: migration from the water column to peripheral biofilms. Environ. Sci. Technol. 42, 5131-5136. doi: 10.1021/es800238e
28. Farkas, A., Butiuc-Keul, A., Ciatarâks, D., Neamktu, C., Crvaciunaks, C., Podar, D., et al. (2013). Microbiological contamination and resistance genes in biofilms occurring during the drinking water treatment process. Sci. Total Environ. 443, 932-938. doi: 10.1016/j.scitotenv.2012.11.068
29. Frost, L. S., Leplae, R., Summers, A. O., and Toussaint, A. (2005). Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3, 722-732. doi: 10.1038/nrmicro1235
30. Fux, C. A., Costerton, J. W., Stewart, P. S., and Stoodley, P. (2005). Survival strategies of infectious biofilms. Trends Microbiol. 13, 34-40. doi: 10.1016/j.tim.2004.11.010
31. Gilbert, P., Maira-Litran, T., McBain, A. J., Rickard, A. H., and Whyte, F. (2002). The physiology and collective recalcitrance of microbial biofilm communities. Adv. Microb. Physiol. 46, 203-256. doi: 10.1016/S0065-2911(02)46005-5
32. Gillings, M., Boucher, Y., Labbate, M., Holmes, A., Krishnan, S., Holley, M., et al. (2008). The evolution of class 1 integrons and the rise of antibiotic resistance. J. Bacteriol. 190, 5095-5100. doi: 10.1128/JB.00152-08
33. Grossart, H. P. (2010). Ecological consequences of bacterioplankton lifestyles: changes in concepts are needed. Environ. Microbiol. Rep. 2, 706-714. doi: 10.1111/j.1758-2229.2010.00179.x
34. Grossart, H. P., Schlingloff, A., Bernhard, M., Simon, M., and Brinkhoff, T. (2004). Antagonistic activity of bacteria isolated from organic aggregates of the German Wadden Sea. FEMS Microbiol. Ecol. 47, 387-396. doi: 10.1016/S0168-6496(03)00305-2
35. Hall-Stoodley, L., Costerton, J. W., and Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2, 95-108. doi: 10.1038/nrmicro821
36. Hausner, M., and Wuertz, S. (1999). High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl. Environ. Microbiol. 65, 3710-3713.
37. Hoffman, L. R., D'Argenio, D. A., MacCoss, M. J., Zhang, Z., Jones, R. A., and Miller, S. I. (2005). Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436, 1171-1175. doi: 10.1038/nature03912
38. Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., and Ciofu, O. (2010). Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35, 322-332. doi: 10.1016/j.ijantimicag.2009.12.011
39. Kent, W. J. (2002). BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664. doi: 10.1101/gr.229202.
40. Liu, B., and Pop, M. (2009). ARDB-Antibiotic Resistance Genes Database. Nucleic Acids Res. 37, D443-D447. doi: 10.1093/nar/gkn656
41. Mah, T. F. C., and O'Toole, G. A. (2001). Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9, 34-39. doi: 10.1016/S0966-842X(00)01913-2
42. Maiques, E., Úbeda, C., Campoy, S., Lasa, I., Novick, R. P., Barbé, J., et al. (2006). β-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. Appl. Environ. Microbiol. 188, 2726-2729.
43. Markowitz, V. M., Chen, I. M., Chu, K., Szeto, E., Palaniappan, K., Grechkin, Y., et al. (2012). IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Res. 40, D123-D129. doi: 10.1093/nar/gkr975
44. Marti, E., Jofre, J., and Balcazar, J. L. (2013). Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS ONE 8:e78906. doi: 10.1371/journal.pone.0078906
45. Marti, E., Variatza, E., and Balcazar, J. L. (2014a). The role of aquatic ecosystems as reservoirs of antibiotic resistance. Trends Microbiol. 22, 36-41. doi: 10.1016/j.tim.2013.11.001
46. Marti, E., Huerta, B., Rodríguez-Mozaz, S., Barceló, D., Jofre, J., and Balcazar, J. L. (2014b). Characterization of ciprofloxacin-resistant isolates from a wastewater treatment plant and its receiving river. Water Res. 61, 67-76. doi: 10.1016/j.watres.2014.05.006
47. Martinez, J. L., Coque, T. M., and Baquero, F. (2015). What is a resistance gene? Ranking risk in resistomes. Nat. Rev. Microbiol. 13, 116-123. doi: 10.1038/nrmicro3399
48. McArthur, A. G., Waglechner, N., Nizam, F., Yan, A., Azad, M. A., Baylay, A. J., et al. (2013). The comprehensive antibiotic resistance database. Antimicrob. Agents Chemother. 57, 3348-3357. doi: 10.1128/AAC.00419-13
49. Meyer, F., Paarmann, D., D'Souza, M., Olson, R., Glass, E. M., Kubal, M., et al. (2008). The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. doi: 10.1186/1471-2105-9-386
50. Miller, C., Thomsen, L. E., Gaggero, C., Mosseri, R., Ingmer, H., and Cohen, S. N. (2004). SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305, 1629-1631. doi: 10.1126/science.1101630
51. Modi, S. R., Collins, J. J., and Relman, D. A. (2014). Antibiotics and the gut microbiota. J. Clin. Invest. 124, 4212-4218. doi: 10.1172/JCI72333
52. Molin, S., and Tolker-Nielsen, T. (2003). Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr. Opin. Biotechnol. 14, 255-261. doi: 10.1016/S0958-1669(03)00036-3
53. Moura, A., Soares, M., Pereira, C., Leitão, N., Henriques, I., and Correia, A. (2009). INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25, 1096-1098. doi: 10.1093/bioinformatics/btp105
54. Nõlvak, H., Truu, M., Tiirik, K., Oopkaup, K., Sildvee, T., Kaasik, A., et al. (2013). Dynamics of antibiotic resistance genes and their relationships with system treatment efficiency in a horizontal subsurface flow constructed wetland. Sci. Total Environ. 46, 636-644. doi: 10.1016/j.scitotenv.2013.05.052
55. Osorio, V., Proia, L., Ricart, M., Pérez, S., Ginebreda, A., Cortina, J. L., et al. (2014). Hydrological variation modulates pharmaceutical levels and biofilm responses in a Mediterranean river. Sci. Total Environ. 472, 1052-1061. doi: 10.1016/j.scitotenv.2013.11.069
56. Parsek, M. R., and Singh, P. K. (2003). Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57, 677-701. doi: 10.1146/annurev.micro.57.030502.090720
57. Proia, L., Morin, S., Peipoch, M., Romaní, A. M., and Sabater, S. (2011). Resistance and recovery of river biofilms receiving short pulses of Triclosan and Diuron. Sci. Total Environ. 409, 3129-3137. doi: 10.1016/j.scitotenv.2011.05.013
58. Proia, L., Osorio, V., Soley, S., Köck-Schulmeyer, M., Pérez, S., Barceló, D., et al. (2013a). Effects of pesticides and pharmaceuticals on biofilms in a highly impacted river. Environ. Pollut. 178, 220-228. doi: 10.1016/j.envpol.2013.02.022
59. Proia, L., Lupini, G., Osorio, V., Pérez, S., Barceló, D., Schwartz, T., et al. (2013b). Response of biofilm bacterial communities to antibiotic pollutants in a Mediterranean river. Chemosphere 92, 1126-1135. doi: 10.1016/j.chemosphere.2013.01.063
60. Pruden, A., Pei, R., Storteboom, H., and Carlson, K. H. (2006). Antibiotic resistance genes as emerging contaminants: studies in northern colorado. Environ. Sci. Technol. 40, 7445-7450. doi: 10.1021/es060413l
61. Ricart, M., Guasch, H., Alberch, M., Barceló, D., Bonnineau, C., Geiszingerb, A., et al. (2010). Triclosan persistence through wastewater treatment plants and its potential toxic effects on river biofilms. Aquat. Toxicol. 100, 346-353. doi: 10.1016/j.aquatox.2010.08.010
62. Romaní, A. M., (2010). "Freshwater biofilms". in Biofouling, eds J. C. Thomason and S. Dürr, (Oxford: Wiley-Blackwell), 137-153.
63. Romero, D., Traxler, M. F., López, D., and Kolter, R. (2011). Antibiotics as signal molecules. Chem. Rev. 111, 5492-5505. doi: 10.1021/cr2000509
64. Roose-Amsaleg, C., and Laverman, A. M. (2015). Do antibiotics have environmental side-effects? Impact of synthetic antibiotics on biogeochemical processes. Environ. Sci. Pollut. Res. doi: 10.1007/s11356-015-4943-3 [Epub ahead of print].
65. Sabater, S., Guasch, H., Ricart, M., Romaní, A., Vidal, G., Klünder, C., et al. (2007). Monitoring the effect of chemicals on biological communities. The biofilm as an interface. Anal. Bioanal. Chem. 387, 1425-1434. doi: 10.1007/s00216-006-1051-8
66. Sabater, S., Guasch, H., Romaní, A., and Muñoz, I. (2002). The effect of biological factors on the efficiency of river biofilms in improving water quality. Hydrobiologia 469, 149-156. doi: 10.1023/A:1015549404082
67. Sabater, S., and Romaní, A. M. (1996). Metabolic changes associated with biofilm formation in an undisturbed Mediterranean stream. Hydrobiologia 335, 107-113. doi: 10.1007/BF00015272
68. Salcedo, D. E., Lee, J. H., Ha, U. H., and Kim, S. P. (2014). The effects of antibiotics on the biofilm formation and antibiotic resistance gene transfer. Desalination Water Treat. 54, 3582-3588. doi: 10.1080/19443994.2014.923206
69. Sarmah, A. K., Meyer, M. T., and Boxall, A. B. A. (2006). A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65, 725-759. doi: 10.1016/j.chemosphere.2006.03.026
70. Schwartz, T., Kohnen, W., Jansen, B., and 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. doi: 10.1111/j.1574-6941.2003.tb01073.x
71. Seiler, C., and Berendonk, T. U. (2012). Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front. Microbiol. 3:399. doi: 10.3389/fmicb.2012.00399
72. Sengupta, S., Chattopadhyay, M. K., and Grossart, H. P. (2013). The multifaceted roles of antibiotics and antibiotic resistance in nature. Front. Microbiol. 4:47. doi: 10.3389/fmicb.2013.00047
73. Sentchilo, V., Mayer, A. P., Guy, L., Miyazaki, R., Green Tringe, S., Barry, K., et al. (2013). Community-wide plasmid gene mobilization and selection. ISME J. 7, 1173-1186. doi: 10.1038/ismej.2013.13
74. Séveno, N. A., Kallifidas, D., Smalla, K., van Elsas, J. D., Collard, J. M., Karagouni, A. D., et al. (2002). Occurrence and reservoirs of antibiotic resistance genes in the environment. Rev. Med. Microbiol. 13, 15-27. doi: 10.1097/00013542-200201000-00002
75. Simon, M., Grossart, H. P., Schweitzer, B., and Ploug, H. (2002). Microbial ecology of organic aggregates in aquatic ecosystems. Aquat. Microb. Ecol. 28, 175-211. doi: 10.3354/ame028175
76. Sobecky, P. A., and Hazen, T. C. (2009). Horizontal gene transfer and mobile genetic elements in marine systems. Methods Mol. Biol. 532, 435-453. doi: 10.1007/978-1-60327-853-9_25
77. Stewart, P. S. (2002). Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 292, 107-113. doi: 10.1078/1438-4221-00196
78. Stewart, P. S., and Costerton, J. W. (2001). Antibiotic resistance of bacteria in biofilms. Lancet 358, 135-138. doi: 10.1016/S0140-6736(01)05321-1
79. Sun, S., Chen, J., Li, W., Altintas, I., Lin, A., Peltier, S., et al. (2011). Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucleic Acids Res. 39, D546-D551. doi: 10.1093/nar/gkq1102
80. Teschler, J. K., Zamorano-Sánchez, D., Utada, A. S., Warner, C. J. A., Wong, G. C. L., Linington, R. G., et al. (2015). Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat. Rev. Microbiol. 13, 255-268. doi: 10.1038/nrmicro3433
81. Vaz-Moreira, I., Nunes, O. C., and Manaia, C. M. (2014). Bacterial diversity and antibiotic resistance in water habitats: searching the links with the human microbiome. FEMS Microbiol. Rev. 38, 761-778. doi: 10.1111/1574-6976.12062
82. Waksman, S. A. (1961). The role of antibiotics in nature. Perspect. Biol. Med. 4, 271-287.
83. Wimpenny, J., Manz, W., and Szewzyk, U. (2000). Heterogeneity in biofilms. FEMS Microbiol. Rev. 24, 661-671. doi: 10.1111/j.1574-6976.2000.tb00565.x
84. Winkworth, C. L. (2013). Antibiotic resistance genes in freshwater biofilms along a whole river. J. Water Health 11, 186-197. doi: 10.2166/wh.2013.223
85. Zhang, W., Sturm, B. S. M., Knapp, C. W., and Graham, D. W. (2009). Accumulation of tetracycline resistance genes in aquatic biofilms due to periodic waste loadings from swine lagoons. Environ. Sci. Technol. 43, 7643-7650. doi: 10.1021/es9014508