Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy
Abstract
:1. Introduction
2. An Overview of Antibiotic Resistance in the Environment
2.1. Resistance Genes in the Environment
2.2. Vectors of ARB Transmission
2.2.1. Surface Waters
2.2.2. Air
2.2.3. Animal Vectors
3. Cytotoxic Effects of Antibiotics in the Environment
3.1. Antibiotic Pollution Disrupts Microbial Communities
3.1.1. Microbial Evolution
3.1.2. Microbial Diversity and Ecosystems Functions
3.2. Antibiotic Pollution and Toxicity in Higher Organisms
3.2.1. Physiological Effects
3.2.2. Effect on Host Microbiomes
4. Policy Approaches to Tackle Antibiotic Pollution and ABR
4.1. Global Context
4.2. Gaps in Current Policies
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Levy, S.B.; Bergman, M.M. The Antibiotic Paradox: How the Misuse of Antibiotics Destroys Their Curative Powers. In Clinical Infectious Diseases, 2nd ed.; Perseus Publishing: Boston, MA, USA, 2003. [Google Scholar]
- Barber, M. Hospital infection yeaterday and today. J. Clin. Pathol. 1961, 14, 2–10. [Google Scholar] [CrossRef] [PubMed]
- Davies, J. Where have all the antibiotics gone? Can. J. Infect. Dis. Med. Microbiol. 2006, 17, 287–290. [Google Scholar] [CrossRef] [PubMed]
- Abraham, E.P.; Chain, E. An enzyme from bacteria able to destroy penicillin. Nature 1940, 146, 837. [Google Scholar] [CrossRef]
- Barber, M.; Rozwadowska-Dowzenko, M. Infection by penicillin-resistant staphylococci. Lancet 1948, 2, 641–642. [Google Scholar] [CrossRef]
- Barber, M. Staphylococcal Infection due to Penicillin-resistant Strains. BMJ 1947, 2, 863–865. [Google Scholar] [CrossRef] [Green Version]
- Smith, J.M.; Feil, E.J.; Smith, N.H. Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 2000, 22, 1115–1122. [Google Scholar] [CrossRef]
- Bush, K.; Courvalin, P.; Dantas, G.; Davies, J.; Eisenstein, B.; Huovinen, P.; Jacoby, G.A.; Kishony, R.; Kreiswirth, B.N.; Kutter, E.; et al. Tackling antibiotic resistance. Nat. Rev. Microbiol. 2011, 9, 894–896. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. Antibiotic Resistance Threats in the United States; Centers for Disease Control and Prevention: Atlanta, GA, USA, 2013.
- Davies, S.C.; Fowler, T.; Watson, J.; Livermore, D.M.; Walker, D. Annual Report of the Chief Medical Officer: Infection and the Rise of Antimicrobial esistance. Lancet 2013, 381, 1606–1609. [Google Scholar] [CrossRef]
- European Centre for Disease Prevention and Control. Joint Report with EMEA: The Bacterial Challange: Time to React. 2011. Available online: https://ecdc.europa.eu/en/publications-data/ecdcemea-joint-technical-report-bacterial-challenge-time-react (accessed on 5 January 2019).
- Livermore, D.M. Discovery research: The scientific challenge of finding new antibiotics. J. Antimicrob. Chemother. 2011, 66, 1941–1944. [Google Scholar] [CrossRef]
- Cohen, M.L. Epidemiology of drug resistance: Implications for a post-antimicrobial era. Science 1992, 257, 1050–1055. [Google Scholar] [CrossRef]
- Neu, H.C. The crisis in antibiotic resistance. Science 1992, 257, 1064–1073. [Google Scholar] [CrossRef] [PubMed]
- Klein, E.Y.; Van Boeckel, T.P.; Martinez, E.M.; Pant, S.; Gandra, S.; Levin, S.A.; Goossens, H.; Laxminarayan, R. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc. Natl. Acad. Sci. USA 2018, 115, E3463–E3470. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Boeckel, T.P.; Brower, C.; Gilbert, M.; Grenfell, B.T.; Levin, S.A.; Robinson, T.P.; Teillant, A.; Laxminarayan, R. Global trends in antimicrobial use in food animals. Proc. Natl. Acad. Sci. USA 2015, 112, 5649–5654. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Henriksson, P.J.G.; Rico, A.; Troell, M.; Klinger, D.H.; Buschmann, A.H.; Saksida, S.; Chadag, M.V.; Zhang, W. Unpacking factors influencing antimicrobial use in global aquaculture and their implication for management: A review from a systems perspective. Sustain. Sci. 2018, 13, 1105–1120. [Google Scholar] [CrossRef] [PubMed]
- Rizzo, L.; Manaia, C.; Merlin, C.; Schwartz, T.; Dagot, C.; Ploy, M.C.; Michael, I.; Fatta-Kassinos, D. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review. Sci. Total Environ. 2013, 447, 345–360. [Google Scholar] [CrossRef] [PubMed]
- Boy-Roura, M.; Mas-Pla, J.; Petrovic, M.; Gros, M.; Soler, D.; Brusi, D.; Menció, A. Towards the understanding of antibiotic occurrence and transport in groundwater: Findings from the Baix Fluvià alluvial aquifer (NE Catalonia, Spain). Sci. Total Environ. 2018, 612, 1387–1406. [Google Scholar] [CrossRef] [PubMed]
- Andersson, D.I.; Hughes, D. Evolution of antibiotic resistance at non-lethal drug concentrations. Drug Resist. Updates 2012, 15, 162–172. [Google Scholar] [CrossRef] [PubMed]
- Kümmerer, K. Antibiotics in the aquatic environment—A review—Part II. Chemosphere 2009, 75, 435–441. [Google Scholar] [CrossRef]
- Finland, M. Emergence of antibiotic resistance in hospitals, 1935–1975. Rev. Infect. Dis. 1979, 1, 4–22. [Google Scholar] [CrossRef]
- Spellberg, B. Antibiotic resistance and antibiotic development. Lancet Infect. Dis. 2008, 8, 211–212. [Google Scholar] [CrossRef]
- Shoemaker, N.B.; Vlamakis, H.; Hayes, K.; Salyers, A.A. Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl. Environ. Microbiol. 2001, 67, 561–568. [Google Scholar] [CrossRef] [PubMed]
- Knapp, C.W.; Dolfing, J.; Ehlert, P.A.I.; Graham, D.W. Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environ. Sci. Technol. 2010, 44, 580–587. [Google Scholar] [CrossRef] [PubMed]
- Walsh, C. Molecular mechanisms that confer antibacterial drug resistance. Nature 2000, 406, 775–781. [Google Scholar] [CrossRef] [PubMed]
- Wright, G. Molecular mechanisms of antibiotic resistance. Chem. Commun. 2011, 47, 4055–4061. [Google Scholar] [CrossRef] [PubMed]
- Gullberg, E.; Cao, S.; Berg, O.G.; Ilbäck, C.; Sandegren, L.; Hughes, D.; Andersson, D.I. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog. 2011, 7, e1002158. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.; Lieberman, T.D.; Kishony, R. Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance. Proc. Natl. Acad. Sci. USA 2014, 111, 14494–14499. [Google Scholar] [CrossRef] [Green Version]
- Haas, D.; Keel, C. Regulation of antibiotic production in root-colonizing Peudomonas spp. and relevance for biological control of plant disease. Ann. Rev. Phytopathol. 2003, 41, 117–153. [Google Scholar] [CrossRef]
- Long, R.A.; Azam, F. Antagonistic Interactions among Marine Pelagic Bacteria. Appl. Environ. Microbiol. 2001, 67, 4975–4983. [Google Scholar] [CrossRef] [Green Version]
- Davies, J. Are antibiotics naturally antibiotics? J. Ind. Microbiol. Biotechnol. 2006, 33, 496–499. [Google Scholar] [CrossRef]
- Goh, E.-B.; Yim, G.; Tsui, W.; McClure, J.; Surette, M.G.; Davies, J. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc. Natl. Acad. Sci. USA 2002, 99, 17025–17030. [Google Scholar] [CrossRef] [Green Version]
- Skindersoe, M.E.; Alhede, M.; Phipps, R.; Yang, L.; Jensen, P.O.; Rasmussen, T.B.; Bjarnsholt, T.; Tolker-Nielsen, T.; Høiby, N.; Givskov, M. Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2008, 52, 3648–3663. [Google Scholar] [CrossRef] [PubMed]
- Aminov, R.I. The role of antibiotics and antibiotic resistance in nature. Environ. Microbiol. 2009, 11, 2970–2988. [Google Scholar] [CrossRef] [PubMed]
- Evans, J.; Dyke, K.G.H. Characterization of the Conjugation System Associated with the Staphylococcus aureus Plasmid pJE1. Microbiology 1988, 134, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, P.Y.; Xu, P.P.; Xia, Z.J.; Wang, J.; Xiong, J.; Li, Y.Z. Combined treatment with the antibiotics kanamycin and streptomycin promotes the conjugation of Escherichia coli. FEMS Microbiol. Lett. 2013, 348, 149–156. [Google Scholar] [CrossRef] [PubMed]
- Bhullar, K.; Waglechner, N.; Pawlowski, A.; Koteva, K.; Banks, E.D.; Johnston, M.D.; Barton, H.A.; Wright, G.D. Antibiotic resistance is prevalent in an isolated cave microbiome. PLoS ONE 2012, 7, e34953. [Google Scholar] [CrossRef] [PubMed]
- D’Costa, V.M. Sampling the Antibiotic Resistome. Science 2006, 311, 374–377. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- D’Costa, V.M.; Osta, V.M.; King, C.E.; Kalan, L.; Morar, M.; Sung, W.W.L.; Schwarz, C.; Froese, D.; Zazula, G.; Calmels, F.; et al. Antibiotic resistance is ancient. Nature 2011, 477, 457–461. [Google Scholar] [CrossRef]
- Perron, G.G.; Whyte, L.; Turnbaugh, P.J.; Goordial, J.; Hanage, W.P.; Dantas, G.; Desai, M.M. Functional characterization of bacteria isolated from ancient arctic soil exposes diverse resistance mechanisms to modern antibiotics. PLoS ONE 2015, 10, e0069533. [Google Scholar] [CrossRef]
- Lee, S.H.; Lee, J.H. Molecular Characterization of TEM-Type beta-Lactamases Identified in Cold-Seep Sediments of Edison Seamount (South of Lihir Island, Papua New Guinea). In Handbook of Molecular Microbial Ecology II: Metagenomics in Different Habitats; Wiley-Blackwell: Hoboken, NJ, USA, 2011; pp. 545–552. [Google Scholar]
- Martínez, J.L. Antibiotics and antibiotic resistance genes in natural environments. Science 2008, 321, 365–367. [Google Scholar] [CrossRef]
- Norman, A.; Hansen, L.H.; Sørensen, S.J. Conjugative plasmids: Vessels of the communal gene pool. Philos. Trans. R. Soc. B Boil. Sci. 2009, 364, 2275–2289. [Google Scholar] [CrossRef]
- Palmer, K.L.; Kos, V.N.; Gilmore, M.S. Horizontal Gene Transfer and the Genomics of Enterococcal Antibiotic Resistance. Curr. Opin. Microbiol. 2011, 13, 632–639. [Google Scholar] [CrossRef] [PubMed]
- Springman, A.C.; Lacher, D.W.; Wu, G.; Milton, N.; Whittam, T.S.; Davies, H.D.; Manning, S.D. Selection, recombination, and virulence gene diversity among group B streptococcal genotypes. J. Bacteriol. 2009, 191, 5419–5427. [Google Scholar] [CrossRef] [PubMed]
- Fournier, P.E.; Vallenet, D.; Barbe, V.; Audic, S.; Ogata, H.; Poirel, L.; Richet, H.; Robert, C.; Mangenot, S.; Abergel, C.; et al. Comparative genomics of multidrug resistance in Acinetobacter baumannii. PLoS Genet. 2006, 2, e7. [Google Scholar] [CrossRef] [PubMed]
- Mazaheri Nezhad Fard, R.; Barton, M.D.; Heuzenroeder, M.W. Bacteriophage-mediated transduction of antibiotic resistance in enterococci. Lett. Appl. Microbiol. 2011, 52, 559–564. [Google Scholar] [CrossRef] [PubMed]
- Colomer-Lluch, M.; Jofre, J.; Muniesa, M. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS ONE 2011, 6, e17549. [Google Scholar] [CrossRef] [PubMed]
- Xu, Z.; Li, L.; Shirtliff, M.E.; Peters, B.M.; Li, B.; Peng, Y.; Alam, M.J.; Yamasaki, S.; Shi, L. Resistance class 1 integron in clinical methicillin-resistant Staphylococcus aureus strains in southern China, 2001–2006. Clin. Microbiol. Infect. 2011, 17, 714–718. [Google Scholar] [CrossRef] [PubMed]
- Machado, E.; Coque, T.M.; Cantón, R.; Sousa, J.C.; Peixe, L. Antibiotic resistance integrons and extended-spectrum β-lactamases among Enterobacteriaceae isolates recovered from chickens and swine in Portugal. J. Antimicrob. Chemother. 2008, 62, 296–302. [Google Scholar] [CrossRef]
- Rowe-Magnus, D.A.; Mazel, D. The role of integrons in antibiotic resistance gene capture. Int. J. Med. Microbiol. 2002, 292, 115–125. [Google Scholar] [CrossRef]
- Gillings, M.R.; Gaze, W.H.; Pruden, A.; Smalla, K.; Tiedje, J.M.; Zhu, Y.G. Using the class 1 integron-integrase gene as a proxy for anthropogenic pollution. ISME J. 2015, 9, 1269–1279. [Google Scholar] [CrossRef]
- Leverstein-van Hall, M.A.; Box, A.T.A.; Blok, H.E.M.; Paauw, A.; Fluit, A.C.; Verhoef, J. Evidence of Extensive Interspecies Transfer of Integron-Mediated Antimicrobial Resistance Genes among Multidrug-Resistant Enterobacteriaceae in a Clinical Setting. J. Infect. Dis. 2002, 186, 49–56. [Google Scholar] [CrossRef]
- Summers, A.O.; Wireman, J.; Vimy, M.J.; Lorscheider, F.L.; Marshall, B.; Levy, S.B.; Bennett, S.; Billard, L. Mercury released from dental ‘silver’ fillings provokes an increase in mercury- and antibiotic-resistant bacteria in oral and intestinal floras of primates. Antimicrob. Agents Chemother. 1993, 37, 825–834. [Google Scholar] [CrossRef] [PubMed]
- Hayashi, S.; Mitsuko, A.; Kimoto, M.; Furukawa, S.; Nakazawa, T. The DsbA-DsbB disulfide bond formation system of Burkholderia cepacia is involved in the production of protease and alkaline phosphatase, motility, metal resistance, and multi-drug resistance. Microbiol. Immunol. 2000, 44, 41–50. [Google Scholar] [CrossRef] [PubMed]
- Baker-Austin, C.; Wright, M.S.; Stepanauskas, R.; McArthur, J.V. Co-selection of antibiotic and metal resistance. Trends Microbiol. 2006, 14, 176–182. [Google Scholar] [CrossRef] [PubMed]
- Chen, B.; Liang, X.; Huang, X.; Zhang, T.; Li, X. Differentiating anthropogenic impacts on ARGs in the Pearl River Estuary by using suitable gene indicators. Water Res. 2013, 47, 2811–2820. [Google Scholar] [CrossRef] [PubMed]
- Ju, F.; Beck, K.; Yin, X.; Maccagnan, A.; McArdell, C.S.; Singer, H.P.; Johnson, D.R.; Zhang, T.; Bürgmann, H. Wastewater treatment plant resistomes are shaped by bacterial composition, genetic exchange, and upregulated expression in the effluent microbiomes. ISME J. 2019, 13, 346–360. [Google Scholar] [CrossRef] [PubMed]
- Graham, D.W.; Knapp, C.W.; Christensen, B.T.; McCluskey, S.; Dolfing, J. Appearance of β-lactam Resistance Genes in Agricultural Soils and Clinical Isolates over the 20 th Century. Sci. Rep. 2016, 6, 21550. [Google Scholar] [CrossRef]
- Pruden, A.; Arabi, M.; Storteboom, H.N. Correlation between upstream human activities and riverine antibiotic resistance genes. Environ. Sci. Technol. 2012, 46, 11541–11549. [Google Scholar] [CrossRef]
- Baquero, F.; Martínez, J.L.; Cantón, R. Antibiotics and antibiotic resistance in water environments. Curr. Opin. Biotechnol. 2008, 19, 260–265. [Google Scholar] [CrossRef]
- Berendonk, T.U.; Manaia, C.M.; Merlin, C.; Fatta-Kassinos, D.; Cytryn, E.; Walsh, F.; Bürgmann, H.; Sørum, H.; Norström, M.; Pons, M.N.; et al. Tackling antibiotic resistance: The environmental framework. Nat. Rev. Microbiol. 2015, 13, 310–317. [Google Scholar] [CrossRef]
- Pitout, J.D.D.; Nordmann, P.; Laupland, K.B.; Poirel, L. Emergence of Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs) in the community. J. Antimicrob. Chemother. 2005, 56, 52–59. [Google Scholar] [CrossRef]
- Breathnach, A.S.; Cubbon, M.D.; Karunaharan, R.N.; Pope, C.F.; Planche, T.D. Multidrug-resistant Pseudomonas aeruginosa outbreaks in two hospitals: Association with contaminated hospital waste-water systems. J. Hosp. Infect. 2012, 82, 19–24. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.H.; Sheng, W.H.; Chang, Y.Y.; Wang, L.H.; Lin, H.C.; Chen, M.L.; Pan, H.J.; Ko, W.J.; Chang, S.C.; Lin, F.Y. Healthcare-associated outbreak due to pan-drug resistant Acinetobacter baumannii in a surgical intensive care unit. J. Hosp. Infect. 2003, 53, 97–102. [Google Scholar] [CrossRef] [PubMed]
- Kizny Gordon, A.E.; Mathers, A.J.; Cheong, E.Y.L.; Gottlieb, T.; Kotay, S.; Walker, A.S.; Peto, T.E.A.; Crook, D.W.; Stoesser, N. The Hospital Water Environment as a Reservoir for Carbapenem-Resistant Organisms Causing Hospital-Acquired Infections—A Systematic Review of the Literature. Clin. Infect. Dis. 2017, 64, 1435–1444. [Google Scholar] [CrossRef] [PubMed]
- Folkesson, A.; Jelsbak, L.; Yang, L.; Johansen, H.K.; Ciofu, O.; Hoiby, N.; Molin, S. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: An evolutionary perspective. Nat. Rev. Microbiol. 2012, 10, 841–851. [Google Scholar] [CrossRef] [PubMed]
- López-Causapé, C.; Rojo-Molinero, E.; Mulet, X.; Cabot, G.; Moyà, B.; Figuerola, J.; Togores, B.; Pérez, J.L.; Oliver, A. Clonal Dissemination, Emergence of Mutator Lineages and Antibiotic Resistance Evolution in Pseudomonas aeruginosa Cystic Fibrosis Chronic Lung Infection. PLoS ONE 2013, 8, e71001. [Google Scholar] [CrossRef] [PubMed]
- Hocquet, D.; Muller, A.; Bertrand, X. What happens in hospitals does not stay in hospitals: Antibiotic-resistant bacteria in hospital wastewater systems. J. Hosp. Infect. 2016, 93, 395–402. [Google Scholar] [CrossRef] [PubMed]
- Reinthaler, F.F.; Posch, J.; Feierl, G.; Wüst, G.; Haas, D.; Ruckenbauer, G.; Mascher, F.; Marth, E. Antibiotic resistance of E. Coli in sewage and sludge. Water Res. 2003, 37, 1685–1690. [Google Scholar] [CrossRef]
- Szczepanowski, R.; Linke, B.; Krahn, I.; Gartemann, K.H.; Gützkow, T.; Eichler, W.; Pühler, A.; Schlüter, A. Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 2009, 155, 2306–2319. [Google Scholar] [CrossRef] [Green Version]
- Bürgmann, H.; Frigon, D.; Gaze, W.H.; Manaia, C.M.; Pruden, A.; Singer, A.C.; Smets, B.F.; Zhang, T. Water and sanitation: An essential battlefront in the war on antimicrobial resistance. FEMS Microbiol. Ecol. 2018, 94, fiy101. [Google Scholar] [CrossRef]
- Yang, Y.; Li, B.; Zou, S.; Fang, H.H.P.; Zhang, T. Fate of antibiotic resistance genes in sewage treatment plant revealed by metagenomic approach. Water Res. 2014, 62, 97–106. [Google Scholar] [CrossRef]
- Chen, H.; Zhang, M. Occurrence and removal of antibiotic resistance genes in municipal wastewater and rural domestic sewage treatment systems in eastern China. Environ. Int. 2013, 55, 9–14. [Google Scholar] [CrossRef] [PubMed]
- Munir, M.; Wong, K.; Xagoraraki, I. Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res. 2011, 45, 681–693. [Google Scholar] [CrossRef] [PubMed]
- Eamens, G.J.; Waldron, A.M. Salmonella uptake in sheep exposed to pastuRes. after biosolids application to agricultural land. Soil Res. 2008, 46, 302–308. [Google Scholar] [CrossRef]
- Diehl, D.L.; Lapara, T.M. Effect of temperature on the fate of genes encoding tetracycline resistance and the integrase of class 1 integrons within anaerobic and aerobic digesters treating municipal wastewater solids. Environ. Sci. Technol. 2010, 44, 9128–9133. [Google Scholar] [CrossRef] [PubMed]
- Chee-Sanford, J.C.; Mackie, R.I.; Koike, S.; Krapac, I.G.; Lin, Y.-F.; Yannarell, A.C.; Maxwell, S.; Aminov, R.I. Fate and Transport of Antibiotic Residues and Antibiotic Resistance Genes following Land Application of Manure Waste. J. Environ. Q. 2009, 38, 1086–1108. [Google Scholar] [CrossRef] [Green Version]
- Ventola, C.L. The antibiotic resistance crisis: Part 1: Causes and threats. Pharm. Ther. J. 2015, 40, 277–283. [Google Scholar]
- Public Health Agency of Canada. Canadian Antimicrobial Resistance Surveillance System—Report 2016. 2016. Available online: https://www.canada.ca/en/public-health/services/publications/drugs-health-products/canadian-antimicrobial-resistance-surveillance-system-report-2016.html (accessed on 5 January 2019).
- Woolhouse, M.; Ward, M.; Van Bunnik, B.; Farrar, J. Antimicrobial resistance in humans, livestock and the wider environment. Philos. Trans. R. Soc. B Boil. Sci. 2015, 370, 20140083. [Google Scholar] [CrossRef]
- Pruden, A.; Pei, R.; Storteboom, H.; Carlson, K.H. Antibiotic resistance genes as emerging contaminants: Studies in northern Colorado. Environ. Sci. Technol. 2006, 40, 7445–7450. [Google Scholar] [CrossRef]
- Peak, N.; Knapp, C.W.; Yang, R.K.; Hanfelt, M.M.; Smith, M.S.; Aga, D.S.; Graham, D.W. Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ. Microbiol. 2007, 9, 143–151. [Google Scholar] [CrossRef]
- Cabello, F.C.; Godfrey, H.P.; Buschmann, A.H.; Dölz, H.J. Aquaculture as yet another environmental gateway to the development and globalisation of antimicrobial resistance. Lancet Infect. Dis. 2016, 16, 127–133. [Google Scholar] [CrossRef]
- Shah, S.Q.A.; Cabello, F.C.; L’Abée-Lund, T.M.; Tomova, A.; Godfrey, H.P.; Buschmann, A.H.; Sørum, H. Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites. Environ. Microbiol. 2014, 16, 1310–1320. [Google Scholar] [CrossRef] [PubMed]
- Buschmann, A.H.; Tomova, A.; López, A.; Maldonado, M.A.; Henríquez, L.A.; Ivanova, L.; Moy, F.; Godfrey, H.P.; Cabello, F.C. Salmon aquaculture and antimicrobial resistance in the marine environment. PLoS ONE 2012, 7, e42724. [Google Scholar] [CrossRef] [PubMed]
- Watts, J.E.M.; Schreier, H.J.; Lanska, L.; Hale, M.S. The rising tide of antimicrobial resistance in aquaculture: Sources, sinks and solutions. Mar. Drugs 2017, 15, 158. [Google Scholar] [CrossRef] [PubMed]
- Larsson, D.G.J. Pollution from drug manufacturing: Review and perspectives. Philos. Trans. R. Soc. B Boil. Sci. 2014, 369, 20130571. [Google Scholar] [CrossRef] [PubMed]
- Larsson, D.G.J.; de Pedro, C.; Paxeus, N. Effluent from drug manufactuRes. contains extremely high levels of pharmaceuticals. J. Hazard. Mater. 2007, 148, 751–755. [Google Scholar] [CrossRef] [PubMed]
- Li, D.; Yang, M.; Hu, J.; Zhang, J.; Liu, R.; Gu, X.; Zhang, Y.; Wang, Z. Antibiotic-resistance profile in environmental bacteria isolated from penicillin production wastewater treatment plant and the receiving river. Environ. Microbiol. 2009, 11, 1506–1517. [Google Scholar] [CrossRef] [PubMed]
- Johnning, A.; Moore, E.R.B.; Svensson-Stadler, L.; Shouche, Y.S.; Joakim Larsson, D.G.; Kristiansson, E. Acquired genetic mechanisms of a multiresistant bacterium isolated from a treatment plant receiving wastewater from antibiotic production. Appl. Environ. Microbiol. 2013, 79, 7256–7263. [Google Scholar] [CrossRef]
- Storteboom, H.; Arabi, M.; Davis, J.G.; Crimi, B.; Pruden, A. Identification of antibiotic-resistance-gene molecular signatuRes. suitable as tracers of pristine River, urban, and agricultural sources. Environ. Sci. Technol. 2010, 44, 1947–1953. [Google Scholar] [CrossRef]
- Graham, D.W.; Olivares-Rieumont, S.; Knapp, C.W.; Lima, L.; Werner, D.; Bowen, E. Antibiotic resistance gene abundances associated with waste discharges to the AlmendaRes. river near Havana, Cuba. Environ. Sci. Technol. 2011, 45, 418–424. [Google Scholar] [CrossRef]
- Pei, R.; Kim, S.C.; Carlson, K.H.; Pruden, A. Effect of River Landscape on the sediment concentrations of antibiotics and corresponding antibiotic resistance genes (ARG). Water Res. 2006, 40, 2427–2435. [Google Scholar] [CrossRef]
- Kristiansson, E.; Fick, J.; Janzon, A.; Grabic, R.; Rutgersson, C.; Weijdegård, B.; Söderström, H.; Joakim Larsson, D.G. Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS ONE 2011, 6, e17038. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Cao, J.; Zhu, Y.G.; Chen, Q.L.; Shen, F.; Wu, Y.; Xu, S.; Fan, H.; Da, G.; Huang, R.J.; et al. Global Survey of Antibiotic Resistance Genes in Air. Environ. Sci. Technol. 2018, 52, 10975–10984. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, J.; Zhao, F.; Zhang, X.X.; Li, K.; Li, C.; Ye, L.; Li, M. Metagenomic profiling of ARGs in airborne particulate matters during a severe smog event. Sci. Total Environ. 2018, 615, 1332–1340. [Google Scholar] [CrossRef]
- Dueker, M.E.; O’Mullan, G.D.; Martínez, J.M.; Juhl, A.R.; Weathers, K.C. Onshore wind speed modulates microbial aerosols along an urban waterfront. Atmosphere 2017, 8, 215. [Google Scholar] [CrossRef]
- Pirnay, J.P.; Bilocq, F.; Pot, B.; Cornelis, P.; Zizi, M.; Van Eldere, J.; Deschaght, P.; Vaneechoutte, M.; Jennes, S.; Pitt, T.; et al. Pseudomonas aeruginosa population structure revisited. PLoS ONE 2009, 4, e7740. [Google Scholar] [CrossRef] [PubMed]
- Hwang, M.S.H.; Morgan, R.L.; Sarkar, S.F.; Wang, P.W.; Guttman, D.S. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 2005, 71, 5182–5191. [Google Scholar] [CrossRef] [PubMed]
- Christner, B.C.; Morris, C.E.; Foreman, C.M.; Cai, R.; Sands, D.C. Ubiquity of biological ice nucleators in snowfall. Science 2008, 319, 1214–1215. [Google Scholar] [CrossRef]
- Li, J.; Zhou, L.; Zhang, X.; Xu, C.; Dong, L.; Yao, M. Bioaerosol emissions and detection of airborne antibiotic resistance genes from a wastewater treatment plant. Atmos. Environ. 2016, 124, 404–412. [Google Scholar] [CrossRef]
- Gao, M.; Jia, R.; Qiu, T.; Han, M.; Wang, X. Size-related bacterial diversity and tetracycline resistance gene abundance in the air of concentrated poultry feeding operations. Environ. Pollut. 2017, 220, 1342–1348. [Google Scholar] [CrossRef]
- McEachran, A.D.; Blackwell, B.R.; Hanson, J.D.; Wooten, K.J.; Mayer, G.D.; Cox, S.B.; Smith, P.N. Antibiotics, bacteria, and antibiotic resistance genes: Aerial transport from cattle feed yards via particulate matter. Environ. Health Perspect. 2015, 123, 337–343. [Google Scholar] [CrossRef]
- Gilbert, Y.; Veillette, M.; Duchaine, C. Airborne bacteria and antibiotic resistance genes in hospital rooms. Aerobiologia 2010, 26, 185–194. [Google Scholar] [CrossRef]
- Bengtsson-Palme, J.; Angelin, M.; Huss, M.; Kjellqvist, S.; Kristiansson, E.; Palmgren, H.; Joakim Larsson, D.G.; Johansson, A. The human gut microbiome as a transporter of antibiotic resistance genes between continents. Antimicrob. Agents Chemother. 2015, 59, 6551–6560. [Google Scholar] [CrossRef] [PubMed]
- Langelier, C.; Graves, M.; Kalantar, K.L.; Caldera, S.; Durrant, R.; Fisher, M.; Backman, R.; Tanner, W.; DeRisi, J.; Leung, D. Microbiome and Antimicrobial Resistance Gene Dynamics in International Travelers. Emerg. Infect. Dis. 2018, 2018, 506394. [Google Scholar] [CrossRef] [PubMed]
- Hanselman, B.A.; Kruth, S.A.; Rousseau, J.; Low, D.E.; Willey, B.M.; McGeer, A.; Weese, J.S. Methicillin-resistant Staphylococcus aureus colonization in veterinary personnel. Emerg. Infect. Dis. 2006, 12, 1933–1938. [Google Scholar] [CrossRef]
- Levy, S.B.; FitzGerald, G.B.; Macone, A.B. Changes in Intestinal Flora of Farm Personnel after Introduction of a Tetracycline-Supplemented Feed on a Farm. N. Engl. J. Med. 1976, 295, 583–588. [Google Scholar] [CrossRef] [PubMed]
- Price, L.B.; Graham, J.P.; Lackey, L.G.; Roess, A.; Vailes, R.; Silbergeld, E. Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers. Environ. Health Perspect. 2007, 115, 1738–1742. [Google Scholar] [CrossRef] [PubMed]
- Levy, S.B. Emergence of antibiotic-resistant bacteria in the intestinal flora of farm inhabitants. J. Infect. Dis. 1978, 137, 688–690. [Google Scholar] [CrossRef]
- Chang, Q.; Wang, W.; Regev-Yochay, G.; Lipsitch, M.; Hanage, W.P. Antibiotics in agriculture and the risk to human health: How worried should we be? Evol. Appl. 2015, 8, 240–247. [Google Scholar] [CrossRef]
- Lis, D.O.; Pacha, J.Z.; Idzik, D. Methicillin resistance of airborne coagulase-negative staphylococci in homes of persons having contact with a hospital environment. Am, J. Infect. Control 2009, 37, 177–182. [Google Scholar] [CrossRef]
- Baran, J.; Ramanathan, J.; Riederer, K.M.; Khatib, R. Stool Colonization With Vancomycin-Resistant Enterococci in Healthcare Workers and Their Households. Infect. Control Hosp. Epidemiol. 2002, 23, 23–26. [Google Scholar] [CrossRef]
- Eveillard, M.; Martin, Y.; Hidri, N.; Boussougant, Y.; Joly-Guillou, M.-L. Carriage of Methicillin-Resistant Staphylococcus aureus Among Hospital Employees: Prevalence, Duration, and Transmission to Households. Infect. Control Hosp. Epidemiol. 2004, 25, 114–120. [Google Scholar] [CrossRef] [PubMed]
- Zurek, L.; Ghosh, A. Insects represent a link between food animal farms and the urban environment for antibiotic resistance traits. Appl. Environ. Microbiol. 2014, 80, 3562–3567. [Google Scholar] [CrossRef] [PubMed]
- Doud, C.W.; Scott, H.M.; Zurek, L. Role of House Flies in the Ecology of Enterococcus faecalis from Wastewater Treatment Facilities. Microb. Ecol. 2014, 67, 380–391. [Google Scholar] [CrossRef] [PubMed]
- Tetteh-Quarcoo, P.B.; Donkor, E.S.; Attah, S.K.; Duedu, K.O.; Afutu, E.; Boamah, I.; Olu-Taiwo, M.; Anim-Baidoo, I.; Ayeh-Kumi, P.F. Microbial Carriage of Cockroaches at a Tertiary Care Hospital in Ghana. Environ. Health Insights 2013, 7, 59–66. [Google Scholar] [CrossRef] [PubMed]
- Tilahun, B.; Worku, B.; Tachbele, E.; Terefe, S.; Kloos, H.; Legesse, W. High load of multi-drug resistant nosocomial neonatal pathogens carried by cockroaches in a neonatal intensive care unit at Tikur Anbessa specialized hospital, AdDis. Ababa, Ethiopia. Antimicrob. Resist. Infect. Control 2012, 1, 12. [Google Scholar] [CrossRef] [PubMed]
- Joyner, C.; Mills, M.K.; Nayduch, D. Pseudomonas aeruginosa in Musca domestica L.: Temporospatial examination of bacteria population dynamics and house fly antimicrobial responses. PLoS ONE 2013, 8, e79224. [Google Scholar] [CrossRef] [PubMed]
- Petridis, M.; Bagdasarian, M.; Waldor, M.K.; Walker, E. Horizontal transfer of Shiga toxin and antibiotic resistance genes among Escherichia coli strains in house fly (Diptera: Muscidae) gut. J. Med. Entomol. 2006, 43, 288–295. [Google Scholar] [CrossRef]
- Vittecoq, M.; Godreuil, S.; Prugnolle, F.; Durand, P.; Brazier, L.; Renaud, N.; Arnal, A.; Aberkane, S.; Jean-Pierre, H.; Gauthier-Clerc, M.; et al. Antimicrobial resistance in wildlife. J. Appl. Ecol. 2016, 53, 519–529. [Google Scholar] [CrossRef] [Green Version]
- Allen, S.E.; Boerlin, P.; Janecko, N.; Lumsden, J.S.; Barker, I.K.; Pear, D.L.; Reid-Smith, R.J.; Jardine, C. Antimicrobial resistance in generic Escherichia coli isolates from wild small mammals living in swine farm, residential, landfill, and natural environments in Southern Ontario, Canada. Appl. Environ. Microbiol. 2011, 77, 882–888. [Google Scholar] [CrossRef]
- Kozak, G.K.; Boerlin, P.; Janecko, N.; Reid-Smith, R.J.; Jardine, C. Antimicrobial resistance in Escherichia coli isolates from Swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl. Environ. Microbiol. 2009, 75, 559–566. [Google Scholar] [CrossRef]
- Marcelino, V.R.; Wille, M.; Hurt, A.C.; Gonzalez-Acuna, D.; Klaassen, M.; Eden, J.-S.; Shi, M.; Iredell, J.R.; Sorrell, T.C.; Holmes, E.C. High levels of antibiotic resistance gene expression among birds living in a wastewater treatment plant. BioRxiv 2018, 2018, 462366. [Google Scholar] [CrossRef]
- Radhouani, H.; Igrejas, G.; Pinto, L.; Gonalves, A.; Coelho, C.; Rodrigues, J.; Poeta, P. Molecular characterization of antibiotic resistance in enterococci recovered from seagulls (Larus cachinnans) representing an environmental health problem. J. Environ. Monit. 2011, 13, 2227–2233. [Google Scholar] [CrossRef] [PubMed]
- Poeta, P.; Radhouani, H.; Igrejas, G.; Gonçalves, A.; Carvalho, C.; Rodrigues, J.; Vinué, L.; Somalo, S.; Torres, C. Seagulls of the Berlengas natural reserve of Portugal as carriers of fecal Escherichia coli harboring CTX-M and TEM extended-spectrum beta-lactamases. Appl. Environ. Microbiol. 2008, 74, 7439–7441. [Google Scholar] [CrossRef] [PubMed]
- Andrews, R.E., Jr.; Johnson, W.S.; Guard, A.R.; Marvin, J.D. Survival of enterococci and Tn 916 -like conjugative transposons in soil. Can. J. Microbiol. 2004, 50, 957–966. [Google Scholar] [CrossRef] [PubMed]
- Jamieson, R.C.; Gordon, R.J.; Sharples, K.E.; Stratton, G.W.; Madani, A. Movement and persistence of fecal bacteria in agricultural soils and subsurface drainage water: A review. Can. Biosyst. Eng. 2002, 44, 1–9. [Google Scholar]
- Avery, L.M.; Williams, A.P.; Killham, K.; Jones, D.L. Survival of Escherichia coli O157:H7 in waters from lakes, rivers, puddles and animal-drinking troughs. Sci. Total Environ. 2008, 389, 378–385. [Google Scholar] [CrossRef]
- Xi, C.; Zhang, Y.; Marrs, C.F.; Ye, W.; Simon, C.; Foxman, B.; Nriagu, J. Prevalence of antibiotic resistance in drinking water treatment and distribution systems. Appl. Environ. Microbiol. 2009, 75, 5714–5718. [Google Scholar] [CrossRef]
- Andersson, D.I.; Levin, B.R. The biological cost of antibiotic resistance. Curr. Opin. Microbiol. 1999, 2, 489–493. [Google Scholar] [CrossRef]
- Andersson, D.I.; Hughes, D. Antibiotic resistance and its cost: Is it possible to reverse resistance? Nat. Rev. Microbiol. 2010, 8, 260–271. [Google Scholar] [CrossRef]
- Schmitt, H.; Stoob, K.; Hamscher, G.; Smit, E.; Seinen, W. Tetracyclines and tetracycline resistance in agricultural soils: Microcosm and field studies. Microb. Ecol. 2006, 51, 267–276. [Google Scholar] [CrossRef]
- Munir, M.; Xagoraraki, I. Levels of Antibiotic Resistance Genes in Manure, Biosolids, and Fertilized Soil. J. Environ. Q. 2011, 40, 248–255. [Google Scholar] [CrossRef] [Green Version]
- Nielsen, K.M.; Smalla, K.; Van Elsas, J.D. Natural transformation of Acinetobacter sp. strain BD413 with cell lysates of Acinetobacter sp., Pseudomonas fluorescens, and Burkholderia cepacia in soil microcosms. Appl. Environ. Microbiol. 2000, 66, 206–212. [Google Scholar] [CrossRef]
- Götz, A.; Smalla, K. Manure enhances plasmid mobilization and survival of Pseudomonas putida introduced into field soil. Appl. Environ. Microbiol. 1997, 63, 1980–1986. [Google Scholar] [PubMed]
- Forsberg, K.J.; Reyes, A.; Wang, B.; Selleck, E.M.; Sommer, M.O.A.; Dantas, G. The shared antibiotic resistome of soil bacteria and human pathogens. Science 2012, 337, 1107–1111. [Google Scholar] [CrossRef] [PubMed]
- Martin, J.F.; Liras, P. Organization and Expression of Genes Involved in the Biosynthesis of Antibiotics and other Secondary Metabolites. Ann. Rev. Microbiol. 2003, 43, 173–206. [Google Scholar] [CrossRef] [PubMed]
- Barlow, M.; Hall, B.G. Experimental prediction of the natural evolution of antibiotic resistance. Genetics 2003, 163, 1237–1241. [Google Scholar] [PubMed]
- Davies, J.; Davies, D. Origins and evolution of antibiotic resistance. Microbiologia 2010, 74, 417–433. [Google Scholar] [CrossRef] [PubMed]
- Yim, G.; Wang, H.H.; Davies, J. Antibiotics as signalling molecules. Philos. Trans. R. Soc. B Boil. Sci. 2007, 362, 1195–1200. [Google Scholar] [CrossRef] [Green Version]
- Hall, B.G.; Barlow, M. Evolution of the serine β-lactamases: Past, present and future. Drug Resist. Updates 2004, 7, 111–123. [Google Scholar] [CrossRef]
- Aminov, R.I.; Mackie, R.I. Evolution and ecology of antibiotic resistance genes. FEMS Microbiol. Lett. 2007, 271, 147–161. [Google Scholar] [CrossRef]
- Martínez, J.L. Effect of antibiotics on bacterial populations: A multi-hierarchical selection process. F1000Research 2017, 6, 51. [Google Scholar] [CrossRef] [PubMed]
- Sanchez-Romero, M.A.; Casadesus, J. Contribution of phenotypic heterogeneity to adaptive antibiotic resistance. Proc. Natl. Acad. Sci. USA 2013, 111, 355–360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El Meouche, I.; Dunlop, M.J. Heterogeneity in efflux pump expression predisposes antibiotic-resistant cells to mutation. Science 2018, 362, 686–690. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, L.; Savage, V.M.; Yeh, P.J. Intermediate Levels of Antibiotics May Increase Diversity of Colony Size Phenotype in Bacteria. Comput. Struct. Biotechnol. J. 2018, 16, 307–315. [Google Scholar] [CrossRef] [PubMed]
- Saxer, G.; Doebeli, M.; Travisano, M. The repeatability of adaptive radiation during long-term experimental evolution of Escherichia coli in a multiple nutrient environment. PLoS ONE 2010, 5, e14184. [Google Scholar] [CrossRef] [PubMed]
- Justice, S.S.; Hunstad, D.A.; Cegelski, L.; Hultgren, S.J. Morphological plasticity as a bacterial survival strategy. Nat. Rev. Microbiol. 2008, 6, 162–168. [Google Scholar] [CrossRef]
- Foster, P. Stress-induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol. 2007, 42, 373–397. [Google Scholar] [CrossRef]
- Andersson, D.I.; Hughes, D. Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol. 2014, 12, 465–478. [Google Scholar] [CrossRef]
- Maiques, E.; Úbeda, C.; Campoy, S.; Salvador, N.; Lasa, Í.; Novick, R.P.; Barbé, J.; Penadés, J.R. β-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 2006, 188, 2726–2729. [Google Scholar] [CrossRef]
- Slager, J.; Kjos, M.; Attaiech, L.; Veening, J.W. Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell 2014, 157, 395–406. [Google Scholar] [CrossRef]
- Davies, J.; Spiegelman, G.B.; Yim, G. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 2006, 9, 445–453. [Google Scholar] [CrossRef] [PubMed]
- Blount, K.F.; Breaker, R.R. Riboswitches as antibacterial drug targets. Nat. Biotechnol. 2006, 24, 1558–1564. [Google Scholar] [CrossRef] [PubMed]
- Rémy, B.; Mion, S.; Plener, L.; Elias, M.; Chabrière, E.; Daudé, D. Interference in bacterial quorum sensing: A biopharmaceutical perspective. Front. Pharmacol. 2018, 9, 203. [Google Scholar] [CrossRef] [PubMed]
- Rice, S. Evolutionary Theory: Mathematical and Conceptual Foundations; Sinauer Associates, Inc.: Boston, MA, USA, 2004. [Google Scholar]
- Lozupone, C.A.; Knight, R. Global patterns in bacterial diversity. Proc. Natl. Acad. Sci. USA 2007, 104, 11436–11440. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Caporaso, J.G.; Lauber, C.L.; Walters, W.A.; Berg-Lyons, D.; Lozupone, C.A.; Turnbaugh, P.J.; Fierer, N.; Knight, R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 2011, 108, 4516–4522. [Google Scholar] [CrossRef] [PubMed]
- Torsvik, V.; Øvreås, L.; Øvreas, L. Microbial Diversity and Function in Soil: From Genes to Ecosystems. Curr. Opin. Microbiol. 2002, 5, 240–245. [Google Scholar] [CrossRef]
- Gibbons, S.M.; Gilbert, J.A. Microbial diversity-exploration of natural ecosystems and microbiomes. Curr. Opin. Genet. Dev. 2015, 35, 66–72. [Google Scholar] [CrossRef] [PubMed]
- Van Bruggen, A.H.C.; Goss, E.M.; Havelaar, A.; van Diepeningen, A.D.; Finckh, M.R.; Morris, J.G. One Health—Cycling of diverse microbial communities as a connecting force for soil, plant, animal, human and ecosystem health. Sci. Total Environ. 2019, 664, 927–937. [Google Scholar] [CrossRef]
- Delcour, A.H. Outer membrane permeability and antibiotic resistance. Biochim. Biophys. Acta Proteins Proteom. 2009, 1794, 808–816. [Google Scholar] [CrossRef] [Green Version]
- Ding, C.; He, J. Effect of antibiotics in the environment on microbial populations. Appl. Microbiol. Biotechnol. 2010, 87, 925–941. [Google Scholar] [CrossRef]
- Eckert, E.M.; Quero, G.M.; Di Cesare, A.; Manfredini, G.; Mapelli, F.; Borin, S.; Fontaneto, D.; Luna, G.M.; Corno, G. Antibiotic disturbance affects aquatic microbial community composition and food web interactions but not community resilience. Mol. Ecol. 2019, 28, 1170–1182. [Google Scholar] [CrossRef]
- Grenni, P.; Ancona, V.; Barra Caracciolo, A. Ecological effects of antibiotics on natural ecosystems: A review. Microchem. J. 2018, 136, 25–39. [Google Scholar] [CrossRef]
- Westergaard, K.; Müller, A.K.; Christensen, S.; Bloem, J.; Sørensen, S.J. Effects of tylosin as a disturbance on the soil microbial community. Soil Biol. Biochem. 2001, 33, 2061–2071. [Google Scholar] [CrossRef]
- Thiele-Bruhn, S.; Beck, I.C. Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 2005, 59, 457–465. [Google Scholar] [CrossRef] [PubMed]
- Cycoń, M.; Mrozik, A.; Piotrowska-Seget, Z. Antibiotics in the Soil Environment—Degradation and Their Impact on Microbial Activity and Diversity. Front. Microbiol. 2019, 10, 338. [Google Scholar] [CrossRef] [PubMed]
- Drury, B.; Scott, J.; Rosi-Marshall, E.J.; Kelly, J.J. Triclosan exposure increases triclosan resistance and influences taxonomic composition of benthic bacterial communities. Environ. Sci. Technol. 2013, 47, 8923–8930. [Google Scholar] [CrossRef] [PubMed]
- Cunha, B.A. Antibiotic side effects. Med. Clin. N. Am. 2001, 85, 149–185. [Google Scholar] [CrossRef]
- Mojica, E.-R.E.; Aga, D.S. Antibiotics Pollution in Soil and Water: Potential Ecological and Human Health Issues. In Encyclopedia of Environmental Health; Elsevier: Burlington, NJ, USA, 2011; pp. 97–110. [Google Scholar]
- Ye, Z.; Weinberg, H.S.; Meyer, M.T. Trace analysis of trimethoprim and sulfonamide, macrolide, quinolone, and tetracycline antibiotics in chlorinated drinking water using liquid chromatography electrospray tandem mass spectrometry. Anal. Chem. 2007, 79, 1135–1144. [Google Scholar] [CrossRef] [PubMed]
- Halden, R.U.; Paull, D.H. Co-occurrence of triclocarban and triclosan in U.S. water resources. Environ. Sci. Technol. 2005, 39, 1420–1426. [Google Scholar] [CrossRef] [PubMed]
- Bever, C.S.; Rand, A.A.; Nording, M.; Taft, D.; Kalanetra, K.M.; Mills, D.A.; Breck, M.A.; Smilowitz, J.T.; German, J.B.; Hammock, B.D. Effects of triclosan in breast milk on the infant fecal microbiome. Chemosphere 2018, 203, 467–473. [Google Scholar] [CrossRef] [PubMed]
- Weatherly, L.M.; Gosse, J.A. Triclosan exposure, transformation, and human health effects. J. Toxicol. Environ. Health Part B Crit. Rev. 2017, 20, 447–469. [Google Scholar] [CrossRef] [PubMed]
- Calafat, A.M.; Ye, X.; Wong, L.Y.; Reidy, J.A.; Needham, L.L. Urinary concentrations of triclosan in the U.S. population: 2003–2004. Environ. Health Perspect. 2008, 116, 303–307. [Google Scholar] [CrossRef] [PubMed]
- Rosi-Marshall, E.J.; Snow, D.; Bartelt-Hunt, S.L.; Paspalof, A.; Tank, J.L. A review of ecological effects and environmental fate of illicit drugs in aquatic ecosystems. J. Hazard. Mater. 2015, 282, 18–25. [Google Scholar] [CrossRef] [PubMed]
- Rosi-Marshall, E.J.; Kelly, J.J. Antibiotic stewardship should consider environmental fate of antibiotics. Environ. Sci. Technol. 2015, 49, 5257–5258. [Google Scholar] [CrossRef] [PubMed]
- Flaherty, C.M.; Dodson, S.I. Effects of pharmaceuticals on Daphnia survival, growth, and reproduction. Chemosphere 2005, 61, 200–207. [Google Scholar] [CrossRef] [PubMed]
- Migliore, L.; Civitareale, C.; Brambilla, G.; Dojmi Di Delupis, G. Toxicity of several important agricultural antibiotics to Artemia. Water Res. 1997, 31, 1801–1806. [Google Scholar] [CrossRef]
- Jung, J.; Kim, Y.; Kim, J.; Jeong, D.H.; Choi, K. Environmental levels of ultraviolet light potentiate the toxicity of sulfonamide antibiotics in Daphnia magna. Ecotoxicology 2008, 17, 37–45. [Google Scholar] [CrossRef]
- Liu, L.; Wu, W.; Zhang, J.; Lv, P.; Xu, L.; Yan, Y. Progress of research on the toxicology of antibiotic pollution in aquatic organisms. Acta Ecol. Sin. 2018, 38, 36–41. [Google Scholar] [CrossRef]
- Wang, H.; Che, B.; Duan, A.; Mao, J.; Dahlgren, R.A.; Zhang, M.; Zhang, H.; Zeng, A.; Wang, X. Toxicity evaluation of β-diketone antibiotics on the development of embryo-larval zebrafish (Danio rerio). Environ. Toxicol. 2014, 29, 1134–1146. [Google Scholar] [CrossRef]
- Lin, T.; Yu, S.; Chen, Y.; Chen, W. Integrated biomarker responses in zebrafish exposed to sulfonamides. Environ. Toxicol. Pharmacol. 2014, 38, 444–452. [Google Scholar] [CrossRef]
- Wang, N.; Noemie, N.; Hien, N.N.; Huynh, T.T.; Silvestre, F.; Phuong, N.T.; Danyi, S.; Widart, J.; Douny, C.; Scippo, M.L.; et al. Adverse effects of enrofloxacin when associated with environmental stress in Tra catfish (Pangasianodon hypophthalmus). Chemosphere 2009, 77, 1577–1584. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Cheng, J.; Xin, Q. Effects of tetracycline on developmental toxicity and molecular responses in zebrafish (Danio rerio) embryos. Ecotoxicology 2015, 24, 707–719. [Google Scholar] [CrossRef] [PubMed]
- Xu, W.; Zhu, X.; Wang, X.; Deng, L.; Zhang, G. Residues of enrofloxacin, furazolidone and their metabolites in Nile tilapia (Oreochromis niloticus). Aquaculture 2006, 254, 1–8. [Google Scholar] [CrossRef]
- Zhang, Y.; Wang, X.; Yin, X.; Shi, M.; Dahlgren, R.A.; Wang, H. Toxicity assessment of combined fluoroquinolone and tetracycline exposure in zebrafish (Danio rerio). Environ. Toxicol. 2016, 31, 736–750. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.Y.; Asselman, J.; Jeong, T.Y.; Yu, S.; De Schamphelaere, K.A.C.; Kim, S.D. Multigenerational Effects of the Antibiotic Tetracycline on Transcriptional Responses of Daphnia magna and Its Relationship to Higher Levels of Biological Organizations. Environ. Sci. Technol. 2017, 51, 12898–12907. [Google Scholar] [CrossRef] [PubMed]
- Jakobsson, H.E.; Jernberg, C.; Andersson, A.F.; Sjölund-Karlsson, M.; Jansson, J.K.; Engstrand, L. Short-term antibiotic treatment has differing long-term impacts on the human throat and gut microbiome. PLoS ONE 2010, 5, e9836. [Google Scholar] [CrossRef] [PubMed]
- Raymann, K.; Moran, N.A. The role of the gut microbiome in health and disease of adult honey bee workers. Curr. Opin. Insect Sci. 2018, 26, 97–104. [Google Scholar] [CrossRef]
- Yan, J.; Herzog, J.W.; Tsang, K.; Brennan, C.A.; Bower, M.A.; Garrett, W.S.; Sartor, B.R.; Aliprantis, A.O.; Charles, J.F. Gut microbiota induce IGF-1 and promote bone formation and growth. Proc. Natl. Acad. Sci. USA 2016, 113, 7554–7563. [Google Scholar] [CrossRef]
- Olszak, T.; An, D.; Zeissig, S.; Vera, M.P.; Richter, J.; Franke, A.; Glickman, J.N.; Siebert, R.; Baron, R.M.; Kasper, D.L.; et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012, 336, 489–493. [Google Scholar] [CrossRef]
- Kong, H.H.; Oh, J.; Deming, C.; Conlan, S.; Grice, E.A.; Beatson, M.A.; Nomicos, E.; Polley, E.C.; Komarow, H.D. NISC Comparative Sequence Program; et al. Temporal shifts in the skin microbiome associated with disease flaRes. and treatment in children with atopic dermatitis. Genome Res. 2012, 22, 850–859. [Google Scholar] [CrossRef]
- Jie, Z.; Xia, H.; Zhong, S.L.; Feng, Q.; Li, S.; Liang, S.; Zhong, H.; Liu, Z.; Gao, Y.; Zhao, H.; et al. The gut microbiome in atherosclerotic cardiovascular disease. Nat. Commun. 2017, 8, 845. [Google Scholar] [CrossRef] [PubMed]
- Qin, J.; Li, Y.; Cai, Z.; Li, S.; Zhu, J.; Zhang, F.; Liang, S.; Zhang, W.; Guan, Y.; Shen, D.; et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012, 490, 55–60. [Google Scholar] [CrossRef] [PubMed]
- Turnbaugh, P.J.; Stintzi, A. Human Health and Disease in a Microbial World. Front. Microbiol. 2011, 2, 190. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Langdon, A.; Crook, N.; Dantas, G. The effects of antibiotics on the microbiome throughout development and alternative approaches for therapeutic modulation. Genome Med. 2016, 8, 39. [Google Scholar] [CrossRef] [PubMed]
- Ianiro, G.; Tilg, H.; Gasbarrini, A. Antibiotics as deep modulators of gut microbiota: Between good and evil. Gut 2016, 65, 1906–1915. [Google Scholar] [CrossRef] [PubMed]
- Schmidt, V.; Amaral-Zettler, L.; Davidson, J.; Summerfelt, S.; Good, C. Influence of Fishmeal-Free Diets on Microbial Communities in Atlantic Salmon (Salmo salar) Recirculation Aquaculture Systems. Appl. Environ. Microbiol. 2016, 82, 4470–4481. [Google Scholar] [CrossRef] [PubMed]
- Schmidt, V.T.; Smith, K.F.; Melvin, D.W.; Amaral-Zettler, L.A. Community assembly of a euryhaline fish microbiome during salinity acclimation. Mol. Ecol. 2015, 24, 2537–2550. [Google Scholar] [CrossRef] [PubMed]
- Navarrete, P.; Mardones, P.; Opazo, R.; Espejo, R.; Romero, J. Oxytetracycline treatment reduces bacterial diversity of intestinal microbiota of Atlantic salmon. J. Aquat. Anim. Health 2008, 20, 177–183. [Google Scholar] [CrossRef]
- Schmidt, V.; Gomez-Chiarri, M.; Roy, C.; Smith, K.; Amaral-Zettler, L. Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish. MSystems 2017, 2, e00133-17. [Google Scholar] [CrossRef] [Green Version]
- Bielen, A.; Šimatović, A.; Kosić-Vukšić, J.; Senta, I.; Ahel, M.; Babić, S.; Jurina, T.; González Plaza, J.J.; Milaković, M.; Udiković-Kolić, N. Negative environmental impacts of antibiotic-contaminated effluents from pharmaceutical industries. Water Res. 2017, 126, 79–87. [Google Scholar] [CrossRef]
- Carlson, J.M.; Leonard, A.B.; Hyde, E.R.; Petrosino, J.F.; Primm, T.P. Microbiome disruption and recovery in the fish Gambusia affinis following exposure to broad-spectrum antibiotic. Infect. Drug Resist. 2017, 10, 143–154. [Google Scholar] [CrossRef] [PubMed]
- Pindling, S.; Azulai, D.; Zheng, B.; Dahan, D.; Perron, G.G. Dysbiosis and early mortality in zebrafish larvae exposed to subclinical concentrations of streptomycin. FEMS Microbiol. Lett. 2018, 365, fny188. [Google Scholar]
- Yan, Z.; Lu, G.; Ye, Q.; Liu, J. Long-term effects of antibiotics, norfloxacin, and sulfamethoxazole, in a partial life-cycle study with zebrafish (Danio rerio): Effects on growth, development, and reproduction. Environ. Sci. Pollut. Res. 2016, 23, 18222–19228. [Google Scholar] [CrossRef] [PubMed]
- Adlard, R.D.; Miller, T.L.; Smit, N.J. The butterfly effect: Parasite diversity, environment, and emerging disease in aquatic wildlife. Trends Parasitol. 2015, 31, 160–166. [Google Scholar] [CrossRef] [PubMed]
- European Comission. A European One Health Action Plan against Antimicrobial Resistance (AMR); European Comission: Brussels, Belgium, 2017. [Google Scholar]
- Public Health Agency of Canada. Tackling Antimicrobial Resistance and Antimicrobial Use: A Pan-Canadian Framework for Action; Public Health Agency of Canada: Ottawa, ON, Canada, 2017.
- Holloway, K.A.; Kotwani, A.; Batmanabane, G.; Puri, M.; Tisocki, K. Antibiotic use in South East Asia and policies to promote appropriate use: Reports from country situational analyses. BMJ 2017, 358, j2291. [Google Scholar] [CrossRef] [PubMed]
- Gandra, S.; Joshi, J.; Trett, A.; Lamkang, A.; Laximinarayan, R. Scoping Report on Antimicrobial Resistance in India; Center for Disease Dynamics, Economics & Policy: Washington, DC, USA, 2017. [Google Scholar]
- Ghafur, A.; Mathai, D.; Muruganathan, A.; Jayalal, J.; Kant, R.; Chaudhary, D.; Prabhash, K.; Abrham, O.; Gopalakrishnan, R.; Ramasubramanian, V.; et al. Chennai Declaration: A solution to the antibiotic resistance in developing countries. Indian J. Cancer 2013, 50, 71–73. [Google Scholar] [CrossRef] [PubMed]
- Government of India. National Action Plan on Antimicrobial Resistance; Government of India: New Delhi, India, 2017.
- Fisheries and Oceans Canada. Aquaculture Activities Regulations Guidance Document. Available online: https://www.dfo-mpo.gc.ca/aquaculture/management-gestion/aar-raa-gd-eng.htm (accessed on 5 January 2019).
- EU Health Policy Platform. Joint Statement of Antimicrobial Resistance (AMR). Available online: https://ec.europa.eu/health/sites/health/files/policies/docs/2017_amr_statement_en.pdf (accessed on 5 January 2019).
- Leonard, A.F.C.; Zhang, L.; Balfour, A.J.; Garside, R.; Gaze, W.H. Human recreational exposure to antibiotic resistant bacteria in coastal bathing waters. Environ. Int. 2015, 82, 92–100. [Google Scholar] [CrossRef] [PubMed]
- United Nations Environment Programme. Frontiers 2017: Eemerging Issues of Environmental Concern; United Nations Environment Programme: Nairobi, Kenya, 2017. [Google Scholar]
- Ashbolt, N.J.; Amézquita, A.; Backhaus, T.; Borriello, P.; Brandt, K.K.; Collignon, P.; Coors, A.; Finley, R.; Gaze, W.H.; Heberer, T.; et al. Human health risk assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environ. Health Perspect. 2013, 121, 993–1001. [Google Scholar] [CrossRef] [PubMed]
Human Medicine | Agriculture/Livestock | Aquaculture | Wastewater Treatment | Pharmaceutical Manufacturing | |
---|---|---|---|---|---|
Canada | + | + | + | - | - |
India | + | - | + | - | - |
Europe | + | + | + | - | - |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kraemer, S.A.; Ramachandran, A.; Perron, G.G. Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy. Microorganisms 2019, 7, 180. https://doi.org/10.3390/microorganisms7060180
Kraemer SA, Ramachandran A, Perron GG. Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy. Microorganisms. 2019; 7(6):180. https://doi.org/10.3390/microorganisms7060180
Chicago/Turabian StyleKraemer, Susanne A., Arthi Ramachandran, and Gabriel G. Perron. 2019. "Antibiotic Pollution in the Environment: From Microbial Ecology to Public Policy" Microorganisms 7, no. 6: 180. https://doi.org/10.3390/microorganisms7060180