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Chapter 9 - Pollution by antibiotics and resistance genes: dissemination into Australian wildlife

Published online by Cambridge University Press:  05 November 2014

By
Michael Gillings
Edited by
Adam Stow ,
Norman Maclean  and
Gregory I. Holwell
Michael Gillings
Affiliation:
Macquarie University
Adam Stow
Affiliation:
Macquarie University, Sydney
Norman Maclean
Affiliation:
University of Southampton
Gregory I. Holwell
Affiliation:
University of Auckland
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Summary

Summary

The effects of antibiotic use and antibiotic resistance are now spreading beyond hospitals and human-dominated landscapes to encompass the whole biosphere. Antibiotics disseminated by waste streams pollute aquatic systems worldwide. These waste streams are also contaminated by bacteria that carry genes for resistance to antibiotics on mobile DNA elements. This circumstance means that aquatic ecosystems are now an evolutionary reactor for DNA rearrangements where novel genes can be assembled into ever more complex DNA elements, and then transferred into a growing diversity of bacterial species. As a consequence, bacteria containing antibiotic resistance genes have now been identified in a range of marine and terrestrial organisms, including wild species and species harvested for human consumption. The dissemination of these resistance genes will have unpredictable consequences for both native organisms and human welfare.

Introduction

Water bodies connect soils, oceans and the atmosphere, and provide essential ecosystem services, but are mostly no longer naturally regulated, since the water cycle has been fundamentally altered by human activity. Further deterioration of water quality is caused by sedimentation, salinisation, eutrophication and contamination with chemical and microbial pollutants (Meybeck 2003). Management of water sources in Australia faces unique challenges as it is the driest inhabited continent on Earth, and is subject to unpredictable variations in rainfall. Extraction of water for human activities is having serious ecological consequences in Australia (Kingsford 2000). Furthermore, water bodies are subject to both diffuse and point sources of pollution from industry, sewage and urban run-off (Francey et al. 2010).

Type
Chapter
Information
Austral Ark
The State of Wildlife in Australia and New Zealand
 , pp. 186 - 196
Publisher: Cambridge University Press
Print publication year: 2014

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References

Allen, H. K., Donato, J., Wang, H. H., et al. (2010) Call of the wild: antibiotic resistance genes in natural environments. Nature Reviews Microbiology 8, 251–9.CrossRefGoogle ScholarPubMed
Arnot, J. A. & Gobas, F. A. P. C. (2004) A food web bioaccumulation model for organic chemicals in aquatic ecosystems. Environmental Toxicology and Chemistry 23, 2343–55.CrossRefGoogle ScholarPubMed
Baker-Austin, C., Wright, M. S., Stepanauskas, R. & McArthur, J. V. (2006) Co-selection of antibiotic and metal resistance. Trends in Microbiology 14, 176–82.CrossRefGoogle ScholarPubMed
Bartoloni, A., Pallecchi, L., Rodríguez, H., et al. (2009) Antibiotic resistance in a very remote Amazonas community. International Journal of Antimicrobial Agents 33, 125–9.CrossRefGoogle Scholar
Boucher, Y., Nesbø, C. L., Joss, M. J., et al. (2006) Recovery and evolutionary analysis of complete integron gene cassette arrays from Vibrio. BMC Evolutionary Biology 6, 3.CrossRefGoogle ScholarPubMed
Chee-Sanford, J. C., Mackie, R. I., Koike, S., et al. (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. Journal of Environmental Qualities 38, 1086–108.CrossRefGoogle ScholarPubMed
Collis, C. M. & Hall, R. M. (1995) Expression of antibiotic resistance genes in the integrated cassettes of integrons. Antimicrobial Agents and Chemotherapy 39, 155–62.CrossRefGoogle ScholarPubMed
Couce, A. & Blázquez, J. (2009) Side effects of antibiotics on genetic variability. FEMS Microbiology Reviews 33, 531–8.CrossRefGoogle ScholarPubMed
Davies, J. & Davies, D. (2010) Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews 74, 417–33.CrossRefGoogle ScholarPubMed
Diamanti-Kandarakis, E., Bourguignon, J.-P., Giudice, L. C., et al. (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocrine Reviews 30, 293–342.CrossRefGoogle Scholar
Domingues, S., Nielsen, K. M. & da Silva, G. J. (2011) The blaIMP-5-carrying integron in a clinical Acinetobacter baumannii strain is flanked by miniature inverted-repeat transposable elements (MITEs). Journal of Antimicrobial Chemotherapy 66, 2667–8.CrossRefGoogle Scholar
Elsaied, H., Stokes, H. W., Kitamura, K., et al. (2011) Marine integrons containing novel integrase genes, attachment sites, attI, and associated gene cassettes in polluted sediments from Suez and Tokyo Bays. The ISME Journal 5, 1162–77.CrossRefGoogle ScholarPubMed
Forsberg, K. J., Reyes, A., Wang, B., et al. (2012) The shared antibiotic resistome of soil bacteria and human pathogens. Science 337, 1107–11.CrossRefGoogle ScholarPubMed
Francey, M., Fletcher, T. D., Deletic, A. & Duncan, H. (2010) New insights into the quality of urban storm water in south eastern Australia. Journal of Environmental Engineering 136, 381–90.CrossRefGoogle Scholar
Garriss, G., Waldor, M. K. & Burrus, V. (2009) Mobile antibiotic resistance encoding elements promote their own diversity. PLoS Genetics 5, e1000775.CrossRefGoogle ScholarPubMed
Gaze, W. H., Abdouslam, N., Hawkey, P. M. & Wellington, E. M. H. (2005) Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrobial Agents and Chemotherapy 49, 1802–7.CrossRefGoogle Scholar
Gaze, W. H., Zhang, L., Abdouslam, N. A., et al. (2011) Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. The ISME Journal 5, 1253–61.CrossRefGoogle ScholarPubMed
Gillings, M. R. (2010) Biocide use, integrons and novel genetic elements. Biocides in the Health Industry 193, 192.Google Scholar
Gillings, M. R. (2013) Evolutionary consequences of antibiotic use for the resistome, mobilome and microbial pangenome. Frontiers in Microbiology 4.CrossRefGoogle ScholarPubMed
Gillings, M. R. & Stokes, H. (2012) Are humans increasing bacterial evolvability?Trends in Ecology & Evolution 27, 346–52.CrossRefGoogle ScholarPubMed
Gillings, M., Boucher, Y., Labbate, M., et al. (2008a) The evolution of class 1 integrons and the rise of antibiotic resistance. Journal of Bacteriology 190, 5095–100.CrossRefGoogle ScholarPubMed
Gillings, M. R., Holley, M. P. & Stokes, H. W. (2009a) Evidence for dynamic exchange of qac gene cassettes between class 1 integrons and other integrons in freshwater biofilms. FEMS Microbiology Letters 296, 282–8.CrossRefGoogle ScholarPubMed
Gillings, M. R., Holley, M. P., Stokes, H. & Holmes, A. J. (2005) Integrons in Xanthomonas: a source of species genome diversity. Proceedings of the National Academy of Sciences of the United States of America 102, 4419–24.CrossRefGoogle ScholarPubMed
Gillings, M. R., Labbate, M., Sajjad, A., et al. (2009b) Mobilization of a Tn402-like class 1 integron with a novel cassette array via flanking miniature inverted-repeat transposable element-like structures. Applied and Environmental Microbiology 75, 6002–4.CrossRefGoogle ScholarPubMed
Gillings, M. R., Xuejun, D., Hardwick, S. A., Holley, M. P. & Stokes, H. W. (2008b) Gene cassettes encoding resistance to quaternary ammonium compounds: a role in the origin of clinical class 1 integrons?The ISME Journal 3, 209–15.CrossRefGoogle ScholarPubMed
Hall, R., Brookes, D. & Stokes, H. (1991) Site-specific insertion of genes into integrons: role of the 59-base element and determination of the recombination cross-over point. Molecular Microbiology 5, 1941–59.CrossRefGoogle ScholarPubMed
Hardwick, S. A., Stokes, H. W., Findlay, S., Taylor, M. & Gillings, M. R. (2008) Quantification of class 1 integron abundance in natural environments using real-time quantitative PCR. FEMS Microbiology Letters 278, 207–12.CrossRefGoogle ScholarPubMed
Heuer, H., Schmitt, H. & Smalla, K. (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Current Opinion in Microbiology 14, 236–43.CrossRefGoogle ScholarPubMed
Holmes, A. J., Holley, M. P., Mahon, A., et al. (2003) Recombination activity of a distinctive integron-gene cassette system associated with Pseudomonas stutzeri populations in soil. Journal of Bacteriology 185, 918–28.CrossRefGoogle ScholarPubMed
Kingsford, R. (2000) Ecological impacts of dams, water diversions and river management on floodplain wetlands in Australia. Austral Ecology 25, 109–27.CrossRefGoogle Scholar
Knapp, C. W., Dolfing, J., Ehlert, P. A. I. & Graham, D. W. (2009) Evidence of increasing antibiotic resistance gene abundances in archived soils since 1940. Environmental Science & Technology 44, 580–7.CrossRefGoogle Scholar
Koenig, J. E., Bourne, D. G., Curtis, B., et al. (2011) Coral-mucus-associated Vibrio integrons in the Great Barrier Reef: genomic hotspots for environmental adaptation. The ISME journal 5, 962–72.CrossRefGoogle ScholarPubMed
Kristiansson, E., Fick, J., Janzon, A., et al. (2011) Pyrosequencing of antibiotic-contaminated river sediments reveals high levels of resistance and gene transfer elements. PLoS ONE 6, e17038.CrossRefGoogle ScholarPubMed
Lapierre, P. & Gogarten, J. P. (2009) Estimating the size of the bacterial pan-genome. Trends in Genetics 25, 107–10.CrossRefGoogle ScholarPubMed
Le-Minh, N., Khan, S. J., Drewes, J. E. & Stuetz, R. M. (2010) Fate of antibiotics during municipal water recycling treatment processes. Water Research 44, 4295–323.CrossRefGoogle ScholarPubMed
Li, D., Yu, T., Zhang, Y., et al. (2010) Antibiotic resistance characteristics of environmental bacteria from an oxytetracycline production wastewater treatment plant and the receiving river. Applied and Environmental Microbiology 76, 3444–51.CrossRefGoogle ScholarPubMed
Lupo, A., Coyne, S. & Berendonk, T. U. (2012) Origin and evolution of antibiotic resistance: the common mechanisms of emergence and spread in water bodies. Frontiers in Microbiology 3.CrossRefGoogle ScholarPubMed
Martinez, J. L. (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environmental Pollution 157, 2893–902.CrossRefGoogle ScholarPubMed
Martinez, J. L. (2012) Natural antibiotic resistance and contamination by antibiotic resistance determinants: the two ages in the evolution of resistance to antimicrobials. Frontiers in Microbiology 3.CrossRefGoogle ScholarPubMed
Meybeck, M. (2003) Global analysis of river systems: from Earth system controls to Anthropocene syndromes. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 358, 1935–55.CrossRefGoogle ScholarPubMed
Moura, A., Henriques, I., Smalla, K. & Correia, A. (2010) Wastewater bacterial communities bring together broad-host range plasmids, integrons and a wide diversity of uncharacterized gene cassettes. Research in Microbiology 161, 58–66.CrossRefGoogle Scholar
Nardelli, M., Scalzo, P. M., Ramírez, M. S., et al. (2012) Class 1 integrons in environments with different degrees of urbanization. PLoS ONE 7, e39223.CrossRefGoogle ScholarPubMed
Nield, B. S., Holmes, A. J., Gillings, M. R., et al. (2001) Recovery of new integron classes from environmental DNA. FEMS Microbiology Letters 195, 59–65.CrossRefGoogle ScholarPubMed
Nield, B. S., Willows, R. D., Torda, A. E., et al. (2004) New enzymes from environmental cassette arrays: functional attributes of a phosphotransferase and an RNA-methyltransferase. Protein Science 13, 1651–9.CrossRefGoogle ScholarPubMed
Palumbi, S. R. (2001) Humans as the world’s greatest evolutionary force. Science 293, 1786–90.CrossRefGoogle ScholarPubMed
Partridge, S. R., Recchia, G. D., Scaramuzzi, C., et al. (2000) Definition of the attI1 site of class 1 integrons. Microbiology 146, 2855–64.CrossRefGoogle ScholarPubMed
Power, M., Emery, S. & Gillings, M. (2013) Into the wild: dissemination of antibiotic resistance dterminants via a species recovery program. PLoS ONE 8, e63017.CrossRefGoogle Scholar
Pruden, A., Larsson, D. J., Amézquita, A., et al. (2013) Management options for reducing the release of antibiotics and antibiotic resistance genes to the environment. Environmental Health Perspectives. .CrossRefGoogle ScholarPubMed
Robinson, A., Wu, P. S.-C., Harrop, S. J., et al. (2005) Integron-associated mobile gene cassettes code for folded proteins: the structure of Bal32a, a new member of the adaptable [alpha]+[beta] barrel family. Journal of Molecular Biology 346, 1229–41.CrossRefGoogle ScholarPubMed
Rockstrom, J., Steffen, W., Noone, K., et al. (2009) Planetary boundaries: exploring the safe operating space for humanity. Ecology and Society 14, 32.CrossRefGoogle Scholar
Rosewarne, C. P., Pettigrove, V., Stokes, H. W. & Parsons, Y. M. (2010) Class 1 integrons in benthic bacterial communities: abundance, association with Tn402-like transposition modules and evidence for coselection with heavy-metal resistance. FEMS Microbiology Ecology 72, 35–46.CrossRefGoogle ScholarPubMed
Sajjad, A., Holley, M. P., Labbate, M., Stokes, H. & Gillings, M. R. (2011) Preclinical class 1 integron with a complete Tn402-like transposition module. Applied and Environmental Microbiology 77, 335–7.CrossRefGoogle ScholarPubMed
Sarmah, A. K., Meyer, M. T. & 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, 725–59.CrossRefGoogle ScholarPubMed
Schlüter, A., Krause, L., Szczepanowski, R., Goesmann, A. & Pühler, A. (2008) Genetic diversity and composition of a plasmid metagenome from a wastewater treatment plant. Journal of Biotechnology 136, 65–76.CrossRefGoogle ScholarPubMed
Schwarzenbach, R. P., Egli, T., Hofstetter, T. B., Von Gunten, U. & Wehrli, B. (2010) Global water pollution and human health. Annual Review of Environment and Resources 35, 109–36.CrossRefGoogle Scholar
Schwarzman, M. R. & Wilson, M. P. (2009) New science for chemicals policy. Science 326, 1065–6.CrossRefGoogle ScholarPubMed
Seiler, C. & Berendonk, T. U. (2012) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Frontiers in Microbiology 3.CrossRefGoogle ScholarPubMed
Siefert, J. L. (2009) Defining the mobilome. In: Horizontal Gene Transfer: Genomes in Flux (eds. Gogarten, M. B., Gogarten, J. P. & Olendzenski, L. C.), pp. 13–27. Humana Press.CrossRefGoogle Scholar
Sjolund, M., Bonnedahl, J., Hernandez, J., et al. (2008) Dissemination of multidrug-resistant bacteria into the Arctic. Emerging Infectious Diseases 14, 70–2.CrossRefGoogle ScholarPubMed
Skurnik, D., Ruimy, R., Andremont, A., et al. (2006) Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. Journal of Antimicrobial Chemotherapy 57, 1215–19.CrossRefGoogle ScholarPubMed
Sorensen, S. J., Bailey, M., Hansen, L. H., Kroer, N. & Wuertz, S. (2005) Studying plasmid horizontal transfer in situ: a critical review. Nature Reviews Microbiology 3, 700–10.CrossRefGoogle ScholarPubMed
Stalder, T., Barraud, O., Casellas, M., Dagot, C. & Ploy, M.-C. (2012) Integron involvement in environmental spread of antibiotic resistance. Frontiers in Microbiology 3.CrossRefGoogle ScholarPubMed
Stokes, H. W. & Gillings, M. R. (2011) Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into Gram-negative pathogens. FEMS Microbiology Reviews 35, 790–819.CrossRefGoogle ScholarPubMed
Stokes, H. & Hall, R. (1989) A novel family of potentially mobile DNA elements encoding site‐specific gene‐integration functions: integrons. Molecular Microbiology 3, 1669–83.CrossRefGoogle ScholarPubMed
Stokes, H., Holmes, A. J., Nield, B. S., et al. (2001) Gene cassette PCR: sequence-independent recovery of entire genes from environmental DNA. Applied and Environmental Microbiology 67, 5240–6.CrossRefGoogle ScholarPubMed
Stokes, H., O’Gorman, D., Recchia, G. D., Parsekhian, M. & Hall, R. M. (1997) Structure and function of 59‐base element recombination sites associated with mobile gene cassettes. Molecular Microbiology 26, 731–45.CrossRefGoogle ScholarPubMed
Storteboom, H., Arabi, M., Davis, J. G., Crimi, B. & Pruden, A. (2010) Identification of antibiotic-resistance-gene molecular signatures suitable as tracers of pristine river, urban, and agricultural sources. Environmental Science and Technology 44, 1947–53.CrossRefGoogle Scholar
Taylor, N. G. H., Verner-Jeffreys, D. W. & Baker-Austin, C. (2011) Aquatic systems: maintaining, mixing and mobilising antimicrobial resistance?Trends in Ecology & Evolution 26, 278–84.CrossRefGoogle ScholarPubMed
Toleman, M. A. & Walsh, T. R. (2011) Combinatorial events of insertion sequences and ICE in Gram-negative bacteria. FEMS Microbiology Reviews 35, 912–35.CrossRefGoogle ScholarPubMed
Watkinson, A. J., Murby, E. J. & Costanzo, S. D. (2007) Removal of antibiotics in conventional and advanced wastewater treatment: Implications for environmental discharge and wastewater recycling. Water Research 41, 4164–76.CrossRefGoogle ScholarPubMed
Wellington, E. M., Boxall, A., Cross, P., et al. (2013) The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. The Lancet Infectious Diseases 13, 155–65.CrossRefGoogle ScholarPubMed
Wright, G. D. (2010) The antibiotic resistome. Expert Opinion in Drug Discovery 5, 779–88.CrossRefGoogle ScholarPubMed
Wright, M. S., Baker-Austin, C., Lindell, A. H., et al. (2008) Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities. The ISME Journal 2, 417–28.CrossRefGoogle ScholarPubMed
Zhang, T., Zhang, X.-X. & Ye, L. (2011) Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLoS ONE 6, e26041.CrossRefGoogle ScholarPubMed

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