Constitutive presence of antibiotic resistance genes within the bacterial community of a large subalpine lake

Molecular Ecology

Volumn 24, Issue 15, 2015, Pages 3888-3900

  Di Cesare, Andrea ^a   Eckert, Ester M ^a   Teruggi, Alessia ^a   Fontaneto, Diego ^a   Bertoni, Roberto ^a   Callieri, Cristiana ^a   Corno, Gianluca ^a  

^a CNR Institute of Ecosystem Study   (Italy)

Author keywords

anthropic impact; antibiotic resistance genes; microbial ecology; quantitative real time PCR; subalpine lakes

Indexed keywords

BACTERIA (MICROORGANISMS);

BACTERIAL DNA;

ANTIBIOTIC RESISTANCE; BACTERIAL GENE; BACTERIUM; DNA SEQUENCE; GENETICS; ITALY; LAKE; MICROBIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SWITZERLAND;

BACTERIA; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; GENES, BACTERIAL; ITALY; LAKES; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SWITZERLAND;

EID: 84937726206     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13293     Document Type: Article

References (85)

1. Ahammad ZS, Sreekrishnan TR, Hands CL, et al,. (2014) Increased waterborne blaNDM-1 resistance gene abundances associated with seasonal human pilgrimages to the upper Ganges River. Environmental Science and Technology, 48, 3014-3020.
2. AIFA (2012) L'uso dei Farmaci in Italia. Rapporto Nazionale. In: OSMED (ed., Farmaco AID,), pp. 209-224. Agenzia Italiana del Farmaco (AIFA), Rome.
3. Ambrosetti V, Barbanti L, Carrara EA, (2010) Mechanism of hypolimnion erosion in a deep lake (Lago Maggiore, N.Italy). Journal of Limnology, 69, 3-14.
4. Amos G, Hawkey P, Gaze W, Wellington E, (2014) Waste water effluent contributes to the dissemination of CTX-M-15 in the natural environment. Journal of Antimicrobial Chemotherapy, 69, 1785-1791.
5. ARCH-Vet. (2013) Bericht über den Vertrieb von Antibiotika in der Veterinärmedizin und das Antibiotikaresistenz monitoring bei Nutztieren in der Schweiz. (ed. Eidgenössisches Departement des Innern BfLuV).
6. Auerbach EA, Seyfried EE, McMahon KD, (2007) Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Research, 41, 1143-1151.
7. Berendonk TU, Manaia CM, Merlin C, et al,. (2015) Tackling antibiotic resistance: the environmental framework. Nature Review Microbiology, 13, 310-317.
8. Bertoni R, Callieri C, Corno G, et al,. (2008) Diversity of epilimnetic and hypolimnetic bacterial communities in a deep Subalpine lake. Cytometry Part A, 73, 67-68.
9. Bertoni R, Callieri C, Corno G, et al,. (2010) Long-term trends of epilimnetic and hypolimnetic bacteria and organic carbon in a deep holo-oligomictic lake. Hydrobiologia, 644, 279-287.
10. Bibbal D, Dupouy V, Ferré J-P, et al,. (2007) Impact of three ampicillin dosage regimens on selection of ampicillin resistance in Enterobacteriaceae and excretion of blaTEM genes in swine feces. Applied and Environmental Microbiology, 73, 4785-4790.
11. Björkman J, Andersson DI, (2000) The cost of antibiotic resistance from a bacterial perspective. Drug Resistance Updates, 3, 237-245.
12. Bonvin F, Rutler R, Chèvre N, Halder J, Kohn T, (2011) Spatial and temporal presence of a wastewater-derived micropollutant plume in Lake Geneva. Environmental Science & Technology, 45, 4702-4709.
13. Börjesson S, Dienues O, Jarnheimer P-Å, et al,. (2009) Quantification of genes encoding resistance to aminoglycosides, β-lactams and tetracyclines in wastewater environments by real-time PCR. International Journal of Environmental Health Research, 19, 219-230.
14. Bustin SA, Benes V, Garson JA, et al,. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry, 55, 611-622.
15. Callieri C, Corno G, Caravati E, et al,. (2009) Bacteria, Archaea, and Crenarchaeota in the epilimnion and hypolimnion of a deep holo-oligomictic lake. Applied and Environmental Microbiology, 75, 7298-7300.
16. Callieri C, Coci M, Eckert EM, Salcher MM, Bertoni R, (2014) Archaea and Bacteria in deep lake hypolimnion: in situ dark inorganic carbon uptake. Journal of Limnology, 73, 31-38.
17. Corno G, Villiger J, Pernthaler J, (2012) Coaggregation in a microbial predator-prey system affects competition and trophic transfer efficiency. Ecology, 94, 870-881.
18. Crawley MJ, (2013) The R Book. John Wiley & Sons, Chichester.
19. 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. Frontiers in Microbiology, 3, 106.
20. Czekalski N, Gascon Diez E, Bürgmann H, (2014) Wastewater as a point source of antibiotic-resistance genes in the sediment of a freshwater lake. ISME Journal, 8, 1381-1390.
21. D'Costa VM, King CE, Kalan L, et al,. (2011) Antibiotic resistance is ancient. Nature, 477, 457-461.
22. Di Cesare A, Luna GM, Vignaroli C, et al,. (2013) Aquaculture can promote the presence and spread of antibiotic-resistant Enterococci in marine sediments. PLoS ONE, 8, e62838.
23. Di Cesare A, Pasquaroli S, Vignaroli C, et al,. (2014) The marine environment as a reservoir of enterococci carrying resistance and virulence genes strongly associated with clinical strains. Environmental Microbiology Reports, 6, 184-190.
24. Durso LM, Cook KL, (2014) Impacts of antibiotic use in agriculture: what are the benefits and risks? Current Opinion in Microbiology, 19, 37-44.
25. Eckert EM, Salcher MM, Posch T, Eugster B, Pernthaler J, (2012) Rapid successions affect microbial N-acetyl-glucosamine uptake patterns during a lacustrine spring phytoplankton bloom. Environmental Microbiology, 14, 794-806.
26. Elliott KT, Cuff LE, Neidle EL, (2013) Copy number change: evolving views on gene amplification. Future Microbiology, 8, 887-899.
27. Engemann CA, Keen PL, Knapp CW, Hall KJ, Graham DW, (2008) Fate of tetracycline resistance genes in aquatic systems: migration from the water column to peripheral biofilms. Environmental Science & Technology, 42, 5131-5136.
28. Enne VI, Livermore DM, Stephens P, Hall L, (2001) Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. The Lancet, 357, 1325-1328.
29. ESVAC (2012) Fourth report. Sales of veterinary antimicrobial agents in 26 EU/EEA countries in 2012.
30. Filippini M, Masiero G, Moschetti K, (2006) Socioeconomic determinants of regional differences in outpatient antibiotic consumption: evidence from Switzerland. Health Policy, 78, 77-92.
31. Graham DW, Olivares-Rieumont S, Knapp CW, et al,. (2011) Antibiotic resistance gene abundances associated with waste discharges to the Almendares River near Havana, Cuba. Environmental Science and Technology, 45, 418-424.
32. Gullberg E, Cao S, Berg OG, et al,. (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathogens, 7, e1002158.
33. Harnisz M, Korzeniewska E, Ciesielski S, Go?as̈ I, (2015) tet genes as indicators of changes in the water environment: relationships between culture-dependent and culture-independent approaches. Science of the Total Environment, 505, 704-711.
34. Hirsch R, Ternes T, Haberer K, Kratz K-L, (1999) Occurrence of antibiotics in the aquatic environment. Science of the Total Environment, 225, 109-118.
35. Holdren JP, Lander E, (2014) Report to the President on combating antibiotic resistance. (ed. (PCAST). PsCoAoSaT), Washington (USA).
36. Jechalke S, Kopmann C, Rosendahl I, et al,. (2013) Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Applied and Environmental Microbiology, 79, 1704-1711.
37. Jones SA, Gibson T, Maltby RC, et al,. (2011) Anaerobic respiration of Escherichia coli in the mouse intestine. Infection and Immunity, 79, 4218-4226.
38. Knapp CW, Dolfing J, Ehlert PA, Graham DW, (2010) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environmental Science and Technology, 44, 580-587.
39. Knapp CW, Lima L, Olivares-Rieumont S, et al,. (2012) Seasonal variations in antibiotic resistance gene transport in the Almendares River, Havana, Cuba. Frontiers in Microbiology, 3, 396.
40. Kümmerer K, (2009) Antibiotics in the aquatic environment-a review-part II. Chemosphere, 75, 435-441.
41. Laanbroek H, Verplanke J, De Visscher P, De Vuyst R, (1985) Distribution of phyto-and bacterioplankton growth and biomass parameters, dissolved inorganic nutrients and free amino acids during a spring bloom in the Oosterschelde basin, The Netherlands. Marine Ecology Progress Series, 25, 1-11.
42. Laht M, Karkman A, Voolaid V, et al,. (2014) Abundances of tetracycline, sulphonamide and beta-lactam antibiotic resistance genes in conventional wastewater treatment plants (WWTPs) with different waste load. PLoS ONE, 9, e103705.
43. LaMarre JM, Locke JB, Shaw KJ, Mankin AS, (2011) Low fitness cost of the multidrug resistance gene cfr. Antimicrobial Agents and Chemotherapy, 55, 3714-3719.
44. Levin BR, Lipsitch M, Perrot V, et al,. (1997) The population genetics of antibiotic resistance. Clinical Infectious Diseases, 24, 9-16.
45. Levy SB, (2002) The Antibiotic Paradox: How the Misuse of Antibiotics Destroys Their Curative Powers. Da Capo Press, Cambridge, Massachusetts.
46. Marti E, Balcázar JL, (2013) Real-time PCR assays for quantification of qnr genes in environmental water samples and chicken feces. Applied and Environmental Microbiology, 79, 1743-1745.
47. Marti E, Jofre J, Balcazar JL, (2013) Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS ONE, 8, e78906.
48. Martinez JL, (2008) Antibiotics and antibiotic resistance genes in natural environments. Science, 321, 365-367.
49. Martinez JL, (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environmental Pollution, 157, 2893-2902.
50. Martinez JL, (2012) Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Frontiers in Microbiology, 3, 1.
51. Martinez JL, Sánchez MB, Martínez-Solano L, et al,. (2009) Functional role of bacterial multidrug efflux pumps in microbial natural ecosystems. Fems Microbiology Reviews, 33, 430-449.
52. Meyer E, Gastmeier P, Deja M, Schwab F, (2013) Antibiotic consumption and resistance: data from Europe and Germany. International Journal of Medical Microbiology, 303, 388-395.
53. Needham DM, Chow C-ET, Cram JA, et al,. (2013) Short-term observations of marine bacterial and viral communities: patterns, connections and resilience. ISME Journal, 7, 1274-1285.
54. Neu HC, (1992) The crisis in antibiotic resistance. Science, 257, 1064-1073.
55. Neuenschwander SM, Pernthaler J, Posch T, Salcher MM, (2014) Seasonal growth potential of rare lake water bacteria suggest their disproportional contribution to carbon fluxes. Environmental Microbiology, 17, 781-795.
56. Ng L-K, Martin I, Alfa M, Mulvey M, (2001) Multiplex PCR for the detection of tetracycline resistant genes. Molecular and Cellular Probes, 15, 209-215.
57. Pasquaroli S, Di Cesare A, Vignaroli C, et al,. (2014) Erythromycin- and copper-resistant Enterococcus hirae from marine sediment and co-transfer of erm(B) and tcrB to human Enterococcus faecalis. Diagnostic Microbiology and Infectious Disease, 80, 26-28.
58. Pei R, Kim S-C, Carlson KH, Pruden A, (2006) Effect of river landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Research, 40, 2427-2435.
59. Prosser JI, Bohannan BJM, Curtis TP, et al,. (2007) The role of ecological theory in microbial ecology. Nature Review Microbiology, 5, 384-392.
60. Pruden A, Larsson DJ, Amézquita A, et al,. (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environmental Health Perspectives, 121, 878-885.
61. R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
62. Rizzo L, Manaia C, Merlin C, et al,. (2013) Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review. Science of the Total Environment, 447, 345-360.
63. Salcher MM, (2013) Same same but different: ecological niche partitioning of planktonic freshwater prokaryotes. Journal of Limnology, 73, 74-87.
64. Salmaso N, Mosello R, (2010) Limnological research in the deep southern subalpine lakes: synthesis, directions and perspectives. Advances in Oceanography and Limnology, 1, 29-66.
65. Salyers AA, Amabile-Cuevas CF, (1997) Why are antibiotic resistance genes so resistant to elimination? Antimicrobial Agents and Chemotherapy, 41, 2321-2325.
66. Schweitzer B, Simon M, (1995) Growth limitation of planktonic bacteria in a large mesotrophic lake. Microbial Ecology, 30, 89-104.
67. Segawa T, Takeuchi N, Rivera A, et al,. (2013) Distribution of antibiotic resistance genes in glacier environments. Environmental Microbiology Reports, 5, 127-134.
68. Sengupta S, Chattopadhyay MK, Grossart H-P, (2013) The multifaceted roles of antibiotics and antibiotic resistance in nature. Frontiers in Microbiology, 4, 47.
69. Sentchilo V, Mayer AP, Guy L, et al,. (2013) Community-wide plasmid gene mobilization and selection. ISME Journal, 7, 1173-1186.
70. Shaffer JP, (1995) Multiple hypothesis testing. Annual Review of Psychology, 46, 561-584.
71. Singer RS, Ward MP, Maldonado G, (2006) Can landscape ecology untangle the complexity of antibiotic resistance? Nature Review Microbiology, 4, 943-952.
72. Stoll C, Sidhu J, Tiehm A, Toze S, (2012) Prevalence of clinically relevant antibiotic resistance genes in surface water samples collected from Germany and Australia. Environmental Science & Technology, 46, 9716-9726.
73. Suzuki MT, Taylor LT, DeLong EF, (2000) Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5′-nuclease assays. Applied and Environmental Microbiology, 66, 4605-4614.
74. Székely AJ, Berga M, Langenheder S, (2012) Mechanisms determining the fate of dispersed bacterial communities in new environments. ISME Journal, 7, 61-71.
75. Tamminen M, Karkman A, Lõhmus A, et al,. (2011) Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. Environmental Science & Technology, 45, 386-391.
76. Taylor NGH, Verner-Jeffreys DW, Baker-Austin C, (2011) Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance? Trends in Ecology & Evolution, 26, 278-284.
77. Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J, (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proceedings of the National Academy of Sciences, USA, 111, 15202-15207.
78. Vaz-Moreira I, Nunes OC, Manaia CM, (2014) Bacterial diversity and antibiotic resistance in water habitats: searching the links with the human microbiome. FEMS Microbiology Reviews, 38, 761-778.
79. Waksman SA, (1961) The role of antibiotics in nature. Perspectives in Biology and Medicine, 4, 271-286.
80. Walsh F, Ingenfeld A, Zampicolli M, et al,. (2011a) Real-time PCR methods for quantitative monitoring of streptomycin and tetracycline resistance genes in agricultural ecosystems. Journal of Microbiological Methods, 86, 150-155.
81. Walsh TR, Weeks J, Livermore DM, Toleman MA, (2011b) Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: An environmental point prevalence study. Lancet Infectious Diseases, 11, 355-362.
82. WHO-World Health Organization (2014) Antimicrobial resistance: global report on surveillance. WHO Report 2014.
83. Wright GD, (2010) Antibiotic resistance in the environment: A link to the clinic? Current Opinion in Microbiology, 13, 589-594.
84. Xi C, Zhang Y, Marrs CF, et al,. (2009) Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Applied and Environmental Microbiology, 75, 5714-5718.
85. Zurfluh K, Hächler H, Nüesch-Inderbinen M, Stephan R, (2013) Characteristics of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae isolates from rivers and lakes in Switzerland. Applied and Environmental Microbiology, 79, 3021-3026.